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Biohybrid actuators for robotics: A review of devices actuated by living cells

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Science Robotics  29 Nov 2017:
Vol. 2, Issue 12, eaaq0495
DOI: 10.1126/scirobotics.aaq0495
  • Fig. 1 Bibliometric analysis of the biohybrid actuation field and few competing ones.

    (A) Papers published from 2006 to 2016 on biohybrid actuators divided in conference papers, journal papers with I.F. <4, journal papers with I.F. between 4 and 10, and journal papers with I.F. >10. The analysis was conducted on the Scopus database by using the following keywords in the title and abstract: “bio-hybrid actuator,” “biohybrid actuator,” “cell-based actuator,” “bioactuation,” “bacteria robot,” “muscle cell actuator,” “muscle-based actuator,” “biohybrid robot,” “bio-hybrid robot,” “biohybrid system,” “bio-hybrid system,” “biohybrid device,” and “bio-hybrid device” (from this list, only the papers closely dealing with bioactuation were then selected manually). (B) Journal papers published from 2006 to 2016 on smart materials–based and pneumatic actuators. The analysis was conducted on the Scopus database by using three different keywords (in title and abstract) for the three categories analyzed: “pneumatic actuator,” “shape memory alloy actuator,” and “electroactive polymer actuator.” (C) Percentage of journal papers with I.F. >4 with respect to the overall number of journal papers published in 2016 on biohybrid actuators, EAP, SMA, and pneumatic actuators.

  • Fig. 2. Examples of application-oriented and nonscalable biohybrid actuators.

    (A) Actuators based on bacteria and other motile cells. (A1) Typical 3D (top) and 2D (bottom) trajectories for bacteria-driven beads (19). Reprinted from (19) with permission from AIP Publishing. (A2) Bacteriobot based on S. typhimurium (top) and its biodistribution in a tumor-bearing mouse (bottom) (21). Reprinted from (21) with permission from Macmillan Publishers Ltd. (A3) Scanning electron microscopy images of unloaded (top left) and liposome-loaded (top right) motile M. marinus and transverse tumor sections of the liposome-loaded microorganism after targeting (bottom) (26). Reprinted from (26) with permission from Macmillan Publishers Ltd. (A4) Representation of a motile sperm cell within a magnetic microtube (top) and its magnetically controlled locomotion at different time points (bottom) (28). (B) Actuators based on explanted whole-muscle tissue. (B1) Image of a swimming robot powered by explanted frog muscles (29). Reprinted from (29) with permission from Wiley. (B2) Fluidic pump powered by an earthworm muscle (30). Reprinted from (30) with permission from Elsevier.

  • Fig. 3 Examples of biohybrid actuators based on mammalian and insect self-contractile cells/tissues.

    (A) Actuators based on cardiomyocytes. (A1) Muscle-powered microdevice based on a muscle bundle self-assembled across two anchors (33). Reproduced from Xi et al. (33) with permission from Macmillan Publishers Ltd. (A2) Concept and prototype of a bioactuated pump (34). Reprinted from (34) with permission from the Royal Society of Chemistry. (A3) Thin elastomeric films with customized functionalities contracted by properly aligned cardiomyocytes (37). Reprinted from (37) with permission from AAAS. (A4) Jellyfish 2D muscle architecture and reverse-engineered medusoid (left), supported by computer simulation (right) (38). Reprinted from (38) with permission from Macmillan Publishers Ltd. (A5) Multilayer hydrogel sheet impregnated with aligned CNT microelectrodes and seeded with cardiomyocytes (40). Reprinted from (35) with permission from Wiley. (A6) Microcylinders contracted by cardiomyocytes seeded on the non-PEGylated side of the microstructures (41). Reprinted from (41) with permission from Wiley. (A7) Biohybrid swimmer powered by cardiomyocytes cultured on its tail (43). Reprinted from (43) with permission from Macmillan Publishers Ltd. (B) Ray fish–mimicking soft robot powered by optogenetically modified cardiomyocytes and controlled through blue light pulses (45). Reprinted from (45) with permission from AAAS. (C) Actuators based on insect self-contractile tissues. (C1) Walking robot powered by insect DVT and operable at room temperature (47). (C2) Microgripper actuated by insect DVT (48). Reprinted from (48) with permission from the Royal Society of Chemistry.

  • Fig. 4 Examples of general-purpose, scalable actuators based on engineered skeletal muscle.

    Different categories are represented: In vitro grown myooids (A), cantilevers/bridges (B), hydrogels and thin films (C), optogenetically modified cells and bioprinted structures (D), and insect embryonic stem cells (E). (A) Myooid engineered in vitro (top), its cross-sectional area (bottom left), and the peak twitch force recorded (bottom right) (50). Reprinted from (50) with permission from Springer. (B) Systems based on cantilevers/bridges. (B1) Contractile myotube assembled on a microfabricated cantilever (53). Reprinted from (53) with permission from Springer. (B2) Si-MEMS device seeded with skeletal muscle cells are able to contract after their differentiation in myotubes (54). Reprinted from (54) with permission from Springer. (B3) One-dimensional PDMS structure populated by myoblasts (55). Reprinted from (55) with permission from the Royal Society of Chemistry. (C) Systems based on engineered hydrogels and thin polymetric substrates. (C1) Ultrathin polylactic acid films cultured with skeletal muscle cells (57). Reprinted from (57) with permission from Springer. (C2) Fibrin gel provided with myotube line patterns and contracted through microelectrode arrays (58). Reprinted from (58) with permission from the Royal Society of Chemistry. (C3) Linear bioactuator based on a 3D rolled PDMS structure cultured with myoblasts (63). (C4) PEDOT/MWCNT sheet cultured with skeletal muscle cells and subjected to crawling-based locomotion (64). (D) Systems based on optogenetically modified cells and bioprinting. (D1) Optogenetically modified skeletal muscle microtissue tethered to elastic force sensors, recording its static and dynamic tension generated after optical stimulation (66). (D2) Top: Modular “ring” design enables ready transfer of skeletal muscle bioactuators to a range of flexible 3D-printed skeletons. Bottom: Light stimulation (left) of an optogenetic muscle-powered biobot drives muscle contraction (middle) and directional locomotion across a substrate (right) (68). (D3) Damaged muscle can self-heal completely within 2 days, restoring bioactuator force production (69). Reprinted from (69) with permission from Wiley. (E) Contractile tissue construct based on larval M. sexta muscle fibers provided with silk sutures and measurement of stress production (73). All images are reproduced or adapted with permission.

  • Fig. 5 Performance of biohybrid actuators and comparison with fully artificial counterparts.

    (A) Actuator force output versus its overall size. (B) Plotting of both artificial and biohybrid actuators in terms of stress produced versus relative stroke. Few references are reported in brackets for biohybrid actuators. (C) Plotting of artificial actuators and natural muscle in terms of power/weight ratio versus actuator efficiency (4). (D) Mass/power ratio, which takes into account both actuator and power source mass, versus actuator autonomous operation time. Some artificial actuation technologies are compared with natural muscle, assuming no periodical feeding (red line) and periodical autonomous feeding (blue line). Data in (C) and (D) reprinted from (4) with permission from Wiley. (E) Lifetimes of “general-purpose” biohybrid actuators reported in the literature for the different categories analyzed in this paper.

Supplementary Materials

  • robotics.sciencemag.org/cgi/content/full/2/12/eaaq0495/DC1

    Movie S1. Biohybrid actuators based on bacteria and other motile cells.

    Movie S2. Biohybrid actuators based on explanted whole-muscle tissues.

    Movie S3. Biohybrid actuators powered by cardiomyocytes.

    Movie S4. Biohybrid actuators based on insect-derived self-contractile tissues.

    Movie S5. Biohybrid actuators based on engineered skeletal muscle.

  • Supplementary Materials

    Supplementary Material for:

    Biohybrid actuators for robotics: A review of devices actuated by living cells

    Leonardo Ricotti,* Barry Trimmer, Adam W. Feinberg, Ritu Raman, Kevin K. Parker, Rashid Bashir, Metin Sitti, Sylvain Martel, Paolo Dario, Arianna Menciassi

    *Corresponding author. Email: leonardo.ricotti{at}santannapisa.it

    Published 29 November 2017, Sci. Robot. 2, eaaq0495 (2017)
    DOI: 10.1126/scirobotics.aaq0495

    This PDF file includes:

    • Legends for movies S1 to S5

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    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mp4 format). Biohybrid actuators based on bacteria and other motile cells.
    • Movie S2 (.mp4 format). Biohybrid actuators based on explanted whole-muscle tissues.
    • Movie S3 (.mp4 format). Biohybrid actuators powered by cardiomyocytes.
    • Movie S4 (.mp4 format). Biohybrid actuators based on insect-derived selfcontractile tissues.
    • Movie S5 (.mp4 format). Biohybrid actuators based on engineered skeletal muscle.

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