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A tissue-engineered jellyfish with biomimetic propulsion

Abstract

Reverse engineering of biological form and function requires hierarchical design over several orders of space and time. Recent advances in the mechanistic understanding of biosynthetic compound materials1,2,3, computer-aided design approaches in molecular synthetic biology4,5 and traditional soft robotics6,7, and increasing aptitude in generating structural and chemical microenvironments that promote cellular self-organization8,9,10 have enhanced the ability to recapitulate such hierarchical architecture in engineered biological systems. Here we combined these capabilities in a systematic design strategy to reverse engineer a muscular pump. We report the construction of a freely swimming jellyfish from chemically dissociated rat tissue and silicone polymer as a proof of concept. The constructs, termed 'medusoids', were designed with computer simulations and experiments to match key determinants of jellyfish propulsion and feeding performance by quantitatively mimicking structural design, stroke kinematics and animal-fluid interactions. The combination of the engineering design algorithm with quantitative benchmarks of physiological performance suggests that our strategy is broadly applicable to reverse engineering of muscular organs or simple life forms that pump to survive.

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References

  1. Mitragotri, S. & Lahann, J. Physical approaches to biomaterial design. Nat. Mater. 8, 15–23 (2009).

    Article  CAS  Google Scholar 

  2. Place, E.S., Evans, N.D. & Stevens, M.M. Complexity in biomaterials for tissue engineering. Nat. Mater. 8, 457–470 (2009).

    Article  CAS  Google Scholar 

  3. von der Mark, K., Park, J., Bauer, S. & Schmuki, P. Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix. Cell Tissue Res. 339, 131–153 (2010).

    Article  CAS  Google Scholar 

  4. Kaznessis, Y.N. Models for synthetic biology. BMC Syst. Biol. 1, 47 (2007).

    Article  CAS  Google Scholar 

  5. Fu, P. A perspective of synthetic biology: assembling building blocks for novel functions. Biotechnol. J. 1, 690–699 (2006).

    Article  CAS  Google Scholar 

  6. Bar-Cohen, Y. EAP as artificial muscles: progress and challenges. Proc. SPIE 5385, 10–16 (2004).

    Article  Google Scholar 

  7. Bar-Cohen, Y. Biomimetics–using nature to inspire human innovation. Bioinspir. Biomim. 1, P1–P12 (2006).

    Article  Google Scholar 

  8. Grosberg, A. et al. Self-organization of muscle cell structure and function. PLOS Comput. Biol. 7, e1001088 (2011).

    Article  CAS  Google Scholar 

  9. Alford, P.W., Feinberg, A.W., Sheehy, S.P. & Parker, K.K. Biohybrid thin films for measuring contractility in engineered cardiovascular muscle. Biomaterials 31, 3613–3621 (2010).

    Article  CAS  Google Scholar 

  10. Huang, A.H., Farrell, M.J. & Mauck, R.L. Mechanics and mechanobiology of mesenchymal stem cell-based engineered cartilage. J. Biomech. 43, 128–136 (2010).

    Article  Google Scholar 

  11. Arai, M.N. A Functional Biology of Scyphozoa (Springer; 1997).

  12. Anderson, P.A.V. & Schwab, W.E. The organization and structure of nerve and muscle in the jellyfish Cyanea capillata (coelenterata; scyphozoa). J. Morphol. 170, 383–399 (1981).

    Article  Google Scholar 

  13. Dabiri, J.O., Colin, S.P., Costello, J.H. & Gharib, M. Flow patterns generated by oblate medusan jellyfish: field measurements and laboratory analyses. J. Exp. Biol. 208, 1257–1265 (2005).

    Article  Google Scholar 

  14. Costello, J.H. & Colin, S.P. Flow and feeding by swimming scyphomedusae. Marine. Biol. 124, 399–406 (1995).

    Article  Google Scholar 

  15. Feitl, K.E., Millett, A.F., Colin, S.P., Dabiri, J.O. & Costello, J.H. Functional morphology and fluid interactions during early development of the scyphomedusa Aurelia aurita. Biol. Bull. 217, 283–291 (2009).

    Article  CAS  Google Scholar 

  16. Nawroth, J.C., Feitl, K.E., Colin, S.P., Costello, J.H. & Dabiri, J.O. Phenotypic plasticity in juvenile jellyfish medusae facilitates effective animal-fluid interaction. Biol. Lett. 6, 389–393 (2010).

    Article  CAS  Google Scholar 

  17. Gladfelter, W.G. A comparative analysis of the locomotory systems of medusoid Cnidaria. Helgol. Wiss. Meeresunters. 25, 228–272 (1973).

    Article  Google Scholar 

  18. Widmer, C.L. How to Keep Jellyfish in Aquariums: An Introductory Guide for Maintaining Healthy Jellies (Wheatmark; 2008).

  19. Gladfelter, W.B. Structure and function of the locomotory system of the Scyphomedusa Cyanea capillata. Marine Biol. 14, 150–160 (1972).

    Article  Google Scholar 

  20. Passano, L.M. Pacemakers and activity patterns the medusae: homage to Romanes. Am. Zool. 5, 465–481 (1965).

    Article  CAS  Google Scholar 

  21. Satterlie, R.A. Neuronal control of swimming in jellyfish: a comparative story. Can. J. Zool. 80, 1654–1669 (2002).

    Article  Google Scholar 

  22. Koehl, M.A. et al. Lobster sniffing: antennule design and hydrodynamic filtering of information in an odor plume. Science 294, 1948–1951 (2001).

    Article  CAS  Google Scholar 

  23. Koehl, M.A.R. Biomechanics of microscopic appendages: functional shifts caused by changes in speed. J. Biomech. 37, 789–795 (2004).

    Article  CAS  Google Scholar 

  24. Chapman, D.M. Microanatomy of the bell rim of Aurelia aurita (Cnidaria: Scyphozoa). Can. J. Zool. 77, 34–46 (1999).

    Article  Google Scholar 

  25. Blanquet, R.S. & Riordan, G.P. An ultrastructural study of the subumbrellar musculature and desmosomal complexes of cassiopea xamachana (Cnidaria: Scyphozoa). Trans. Am. Microsc. Soc. 100, 109–119 (1981).

    Article  Google Scholar 

  26. Hayward, R.T. Modeling Experiments on Pacemaker Interactions in Scyphomedusae. PhD thesis, UNCW 〈http://libres.uncg.edu/ir/uncw/listing.aspx?id=1787〉 (2007).

  27. Grosberg, A., Alford, P.W., McCain, M.L. & Parker, K.K. Ensembles of engineered cardiac tissues for physiological and pharmacological study: heart on a chip. Lab Chip 11, 4165–4173 (2011).

    Article  CAS  Google Scholar 

  28. Böl, M., Reese, S., Parker, K.K. & Kuhl, E. Computational modeling of muscular thin films for cardiac repair. Comput. Mech. 43, 535–544 (2008).

    Article  Google Scholar 

  29. Shim, J., Grosberg, A., Nawroth, J.C., Parker, K.K. & Bertoldi, K. Modeling of cardiac muscular thin films: pre-stretch, passive and active behavior. J. Biomech. 45, 832–841 (2012).

    Article  Google Scholar 

  30. Feinberg, A.W. et al. Muscular thin films for building actuators and powering devices. Science 317, 1366–1370 (2007).

    Article  CAS  Google Scholar 

  31. Marder, M., Deegan, R. & Sharon, E. Crumpling, buckling, and cracking: elasticity of thin sheets. Phys. Today 60, 33–38 (2007).

    Article  Google Scholar 

  32. Vogel, S. Life in Moving Fluids: the Physical Biology of Flow (Princeton University Press, 1996).

  33. Fedorov, V.V. et al. Application of blebbistatin as an excitation-contraction uncoupler for electrophysiologic study of rat and rabbit hearts. Heart Rhythm 4, 619–626 (2007).

    Article  Google Scholar 

  34. Bayly, P.V. et al. Estimation of conduction velocity vector fields from epicardial mapping data. IEEE Trans. Biomed. Eng. 45, 563–571 (1998).

    Article  CAS  Google Scholar 

  35. Bray, M.-A., Sheehy, S.P. & Parker, K.K. Sarcomere alignment is regulated by myocyte shape. Cell Motil. Cytoskeleton 65, 641–651 (2008).

    Article  Google Scholar 

  36. Hamley, I.W. Liquid crystals. in Introduction to Soft Matter: Synthetic and Biological Self-Assembling Materials, pp. 221–273 (John Wiley & Sons, 2007) 〈http://onlinelibrary.wiley.com/doi/10.1002/9780470517338.ch5/summary〉.

  37. Umeno, A. & Ueno, S. Quantitative analysis of adherent cell orientation influenced by strong magnetic fields. IEEE Trans. Nanobioscience 2, 26–28 (2003).

    Article  Google Scholar 

  38. Satheesh, V.K., Chhabra, R.P. & Eswaran, V. Steady incompressible fluid flow over a bundle of cylinders at moderate Reynolds numbers. Can. J. Chem. Eng. 77, 978–987 (1999).

    Article  CAS  Google Scholar 

  39. Masliyah, J.H. & Epstein, N. Steady symmetric flow past elliptical cylinders. Ind. Eng. Chem. Fundam. 10, 293–299 (1971).

    Article  CAS  Google Scholar 

  40. Halliday, D., Resnick, R. & Walker, J. Fundamentals of Physics (John Wiley and Sons, 2010).

  41. Adrian, R.J. Particle-imaging techniques for experimental fluid mechanics. Annu. Rev. Fluid Mech. 23, 261–304 (1991).

    Article  Google Scholar 

  42. Willert, C.E. & Gharib, M. Digital particle image velocimetry. Exp. Fluids 10, 181–193 (1991).

    Article  Google Scholar 

  43. Abramoff, M., Magelhaes, P. & Ram, S. Image processing with ImageJ. Biophotonics Int. 11, 36–42 (2004).

    Google Scholar 

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Acknowledgements

We acknowledge financial support from the Wyss Institute for Biologically Inspired Engineering at Harvard, the Harvard Materials Research Science and Engineering Center under National Science Foundation award number DMR-0213805, US National Institutes of Health grant 1 R01 HL079126 (K.K.P.), and from the office of Naval Research and National Science Foundation Program in Fluid Dynamics (J.O.D.). We acknowledge the Harvard Center for Nanoscale Science for use of facilities and the New England Aquarium for supplying jellyfish. We thank J. Goss, P.W. Alford, K.R. Sutherland, K. Balachandran, C. Regan, P. Campbell, S. Spina and A. Agarwal for comments and technical support.

Author information

Authors and Affiliations

Authors

Contributions

K.K.P., J.O.D. and J.C.N. conceived the project, designed the experiments and prepared the manuscript. J.O.D. and J.C.N. developed the fluid model. J.C.N. did the experiments and analyzed the data. H.L., A.W.F., C.M.R., M.L.M. and A.G. supervised experiments, analyzed data and gave conceptual advice. M.L.M. isolated rat cardiomyocytes for experiments.

Corresponding authors

Correspondence to John O Dabiri or Kevin Kit Parker.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Methods and Supplementary Figs. 1-8 (PDF 6118 kb)

Supplementary Movie 1

This movie shows the stroke cycle in a free-swimming juvenile Moon jellyfish (Aurelia aurita)consisting of muscle-powered contraction (power stroke) and elastic recoil (recovery stroke) (MOV 4232 kb)

Supplementary Movie 2

This movie shows the failure of a biomimetic Medusoid design to propel itself. The Medusoidconstruct was paced at 1 Hz through an externally applied monophasic square pulse (2.5V/cm,10ms duration). Due to mismatch of muscle stresses and substrate compliance, musclecontraction does not result in sufficient bell deformation, and no thrust is generated (MOV 1473 kb)

Supplementary Movie 3

This movie demonstrates jellyfish-like body contraction and free-swimming of optimallydesigned Medusoid constructs. Medusoids were paced at 1 Hz through an externally appliedmonophasic square pulse (2.5V/cm, 10ms duration). The first scene shows a mature constructstill attached at its center to its casting mold, just prior to release. (Note that the striatedappearance of the casting mold is caused by its fabrication process; in particular, this striationdoes not reflect the alignment of the muscle tissue on top of the silicone membrane covering themold). Subsequent scenes show exemplary propulsion of free-swimming Medusoids (MOV 5675 kb)

Supplementary Movie 4

This movie demonstrates comparative propulsion efficacy (distance per stroke) in jellyfish andoptimal Medusoids, whereas suboptimal Medusoids (“sieve design”) exhibit inferiorperformance. While Medusoids were paced at 1 Hz through an externally applied electric field of6 V, here the jellyfish contracts at a frequency of ca. 2 Hz. In order to facilitate comparison, theframe rate of the jellyfish recording was halved to synchronize stroke phases (MOV 2731 kb)

Supplementary Movie 5

This movie shows a sequence of raw DPIV data for jellyfish, Medusoid and suboptimally (=sieve-) designed Medusoids. Here, fluid flow around the jellyfish/Medusoid bell is visualized by the displacement of neutrally buoyant particles suspended within the fluid and illuminatedwithin a single plane using laser light. The relative motion of the particles allows quantifying 2Dfluid flow within the plane (MOV 2997 kb)

Supplementary Movie 6

This movie shows the fluid flow field and the vorticity field of a juvenile jellyfish during thestroke cycle. The movie was generated from DPIV data. The power stroke is characterized bymaximal fluid velocities and formation of a starting vortex, generating thrust. The recoverystroke is characterized by reduced fluid velocities and the formation of a stopping vortex,generating feeding currents towards the subumbrellar side (MOV 5745 kb)

Supplementary Movie 7

This movie shows the fluid flow field and the vorticity field of an optimally designed Medusoidduring the stroke cycle. The movie was generated from DPIV data. As in the jellyfish, the powerstroke generates maximal fluid velocities and a starting vortex ring, resulting in thrust. Therecovery stroke generates a stopping vortex ring that draws feeding currents towards the subumbrella (MOV 4993 kb)

Supplementary Movie 8

This movie shows the fluid flow field and the vorticity field of a suboptimal Medusoid design.The movie was generated from DPIV data. In contrast to jellyfish and optimal Medusoids,suboptimal Medusoids with “sieve design” fail to sufficiently accelerate fluid during the powerstroke, resulting in poor thrust generation. Vorticity patterns are more diffuse compared to thoseobserved in jellyfish and optimal designs, and further flow analysis revealed that generation offeeding currents was inferior as well (Fig. 4) (MOV 6131 kb)

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Nawroth, J., Lee, H., Feinberg, A. et al. A tissue-engineered jellyfish with biomimetic propulsion. Nat Biotechnol 30, 792–797 (2012). https://doi.org/10.1038/nbt.2269

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