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In This Article

  • Summary
  • Abstract
  • Introduction
  • Protocol
  • Representative Results
  • Discussion
  • Acknowledgements
  • Materials
  • References
  • Reprints and Permissions

Summary

A bioinspired scaffold is fabricated by a soft photolithography technique using mechanically robust and electrically conductive hydrogels. The micropatterned hydrogels provide directional cardiomyocyte cell alignment, resulting in a tailored direction of actuation. Flexible microelectrodes are also integrated into the scaffold to bring electrical controllability for a self-actuating cardiac tissue.

Abstract

Bioinspired soft robotic systems that mimic living organisms using engineered muscle tissue and biomaterials are revolutionizing the current biorobotics paradigm, especially in biomedical research. Recreating artificial life-like actuation dynamics is crucial for a soft-robotic system. However, the precise control and tuning of actuation behavior still represents one of the main challenges of modern soft robotic systems. This method describes a low-cost, highly scalable, and easy-to-use procedure to fabricate an electrically controllable soft robot with life-like movements that is activated and controlled by the contraction of cardiac muscle tissue on a micropatterned sting ray-like hydrogel scaffold. The use of soft photolithography methods makes it possible to successfully integrate multiple components in the soft robotic system, including micropatterned hydrogel-based scaffolds with carbon nanotubes (CNTs) embedded gelatin methacryloyl (CNT-GelMA), poly(ethylene glycol) diacrylate (PEGDA), flexible gold (Au) microelectrodes, and cardiac muscle tissue. In particular, the hydrogels alignment and micropattern are designed to mimic the muscle and cartilage structure of the sting ray. The electrically conductive CNT-GelMA hydrogel acts as a cell scaffold that improves the maturation and contraction behavior of cardiomyocytes, while the mechanically robust PEGDA hydrogel provides structural cartilage-like support to the whole soft robot. To overcome the hard and brittle nature of metal-based microelectrodes, we designed a serpentine pattern that has high flexibility and can avoid hampering the beating dynamics of cardiomyocytes. The incorporated flexible Au microelectrodes provide electrical stimulation across the soft robot, making it easier to control the contraction behavior of cardiac tissue.

Introduction

Modern state-of-the-art soft robots can mimic the hierarchical structures and muscle dynamics of many living organisms, such as the jellyfish1,2, sting ray2, octopus3, bacteria4, and sperm5. Mimicking the dynamics and architecture of natural systems offers higher performances in terms of both energetic and structural efficiency6. This is intrinsically related to the soft nature of natural tissue (e.g., skin or muscle tissue with a Young's modulus between 104−109

Protocol

This study was carried out in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. The protocol was approved by the institutional Animal Care and Use Committee (IACUC) of Brigham and Women's Hospital.

1. GelMA synthesis

  1. Dissolve 10 g of gelatin in 100 mL of Dulbecco's phosphate-buffered saline (DPBS) using a magnetic stirrer at 50 °C.
  2. Add 8 mL of methacrylic anhydride slowly w.......

Representative Results

Flow diagram of the steps for developing the Au microelectrode-incorporated bioinspired soft robot
The aim of the soft robot design was to build a membrane capable of actuating a swimming movement with minimal complexity. The structure must be able to sustain strong flexions repeatedly over time (about 1 Hz) and be able to keep its shape while achieving a strong beating. By selectively photo crosslinking the polymer using photomasks, we fabricated a hierarchically structured scaffold comprised of a.......

Discussion

Using this method, we were able to successfully fabricate a batoid fish-like bioinspired soft robot with an integrated self-actuating cardiac tissue on a multilayer structured scaffold that is controlled by embedded Au microelectrodes. Due to two distinct micropatterned hydrogel layers made of PEGDA and CNT–GelMA hydrogels, the bioinspired scaffold showed good mechanical stability and ideal cell alignment and maturation. The PEGDA pattern layer, which serves as a cartilage joint of the skeletal architecture in a st.......

Acknowledgements

This paper was funded by the National Institutes of Health (R01AR074234, R21EB026824, R01 AR073822-01), the Brigham Research Institute Stepping Strong Innovator Award, and AHA Innovative Project Award (19IPLOI34660079).

....

Materials

NameCompanyCatalog NumberComments
250 mL BeakerPYREX1000-250CNEa
2-Hydroxy-4'-(2-hydroxyethoxy)-2-methylpropiophenoneSigma-Aldrich410896
3-(Trimethoxysilyl)propyl methacrylateMiliporeM6514
37° Water bathVWRW6M
4',6-diamidino-2-phenylindole (DAPI)Sigma-AldrichD9542
50mL Conical Centrifuge TubesFalcon14-959-49A
70 µm Cell StrainerFalcon352350
80° incubatorVWR1370GM
Alexa Fluor 488 goat anti-mouse IgG (H+L)InvitrogenA11029
Alexa Fluor 594 goat anti-rabbit IgG (H+L)InvitrogenA11037
Alexa Fluor 488 PhalloidinInvitrogenA12379
Antibiotic/Antimycotic solutionThermoFisher Scientific15240062
Anti-Connexin 43/GJAI antibodyAbcamab11370Rabbit polyclonal
Anti-Sarcomeric α-actininAbcamab9465Mouse monoclonal
Benchtop Freeze DryersLabconco77500-00 K
Biosafety cabinetSterilgardA/B3
Carbon rod electrodesSGL Carbon Group6971105
CentrifugeEppendorf5804
CO2 incubatorForma Scientific3110
Collagenase, Type II, PowderGibco17-101-015
Confocal MicroscopeZeissLSM 880
COOH Functionalized Carbon NanotubesNanoLabPD30L5-20-COOH
Dicing saw machineGiorgio TechnologyDAD-321
DMEM, High GlucoseGibco11-965-118
DPBS without Calcium and MagnesiumGibco14-190-144
E-beam evaporatorCHA57367
Fetal Bovine SerumGibco10-437-028
GelatinSigma-AldrichG9391Type B, 300 bloom from porcine skin
Glass slideVWR48382-180
HBSS without Calcium, Magnesium or Phenol RedGibco14-175-079
Inverted optical microscopeOlympusCK40
Magnetic hotplateCorningPC-420
methacrylic anhydrideSigma-Aldrich276695Contains 2,000ppm topanol A as inhibitor
Nunc EasYFlask 175cm2ThermoFisher Scientific159910
OlicscopeSiglentSDS1052DL+
Paraformaldehyde Aqueous Solution -16%Electron Microscopy Sciences15710
PDMS SYLGARD 184Sigma-Aldrich761036
PhotomaskMini micro stencil inc
Platinum wireAlfa AesarAA43014BU
Polyethylene glycol dimethcrylatePolysciences Inc.15178-100
Regenerated Cellulose Dialysis TubingFisherbrand21-152-14
Silver Epoxy AdhesiveMG Chemicals8330S
Stericup Quick Release-GP Sterile Vacuum Filtration SystemMilliporeS2GPU02RE
Ultra sonicatorQsonicaQ500
UV Curing SystemOmniCureS2000
Vortex mixerScientific IndustrySI-0246A
Waveform generatorAgilent33500B
Wrap Aluminium foilReynoldsN/A

References

  1. Nawroth, J. C., et al. A tissue-engineered jellyfish with biomimetic propulsion. Nature Biotechnology. 30 (8), 792-797 (2012).
  2. Park, S. J., et al. Phototactic guidance of a tissue-engineered soft-robotic ray.

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BioinspiredSoft RobotMicroelectrodesBiohybrid ActuatorCell based ActuatorGelMACarbon NanotubesPEGDAMicropatterningGold MicroelectrodesCardiomyocytesElectrical StimulationHeart Regeneration

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