An autonomously swimming biohybrid fish designed with human cardiac biophysics

• Type of Material: Article
• Authors: Keel Y Lee, Harvard University; Sung Jin Park, Emory University; David G Matthews, Harvard University; Sean L Kim, Harvard University; Carlos A Marquez, Harvard University; John F Zimmerman, Harvard University; Herdeline AM Ardoña, Harvard University; Andre G Kleber, Harvard Medical School; George Lauder, Harvard University; Kevin Kit Parker, Harvard University
• Language: English
• Date: 2022-02-11
• Publisher: AMER ASSOC ADVANCEMENT SCIENCE
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
• Final Published Version (URL): http://dx.doi.org/10.1126/science.abh0474
• Title of Journal or Parent Work: SCIENCE
• Volume: 375
• Issue: 6581
• Start Page: 639
• End Page: +
• Grant/Funding Information: The views and conclusions contained in this document are those of the authors and should not be interpreted as representing the official policies, either expressed or implied, of the National Institutes of Health, the National Science Foundation, or the US Government.; G.V.L. was funded by the Office of Naval Research (T. McKenna, Program Manager, ONR 341), grant N00014-15-1-2234, and the National Science Foundation, grant 1830881. H.A.M.A. would like to thank the American Chemical Society for their generous support through the Irving S. Sigal Postdoctoral Fellowship.; this work was funded by the Harvard Paulson School of Engineering and Applied Sciences, the Wyss Institute for Biologically Inspired Engineering, National Institutes of Health National Center for Advancing Translational Sciences grant UH3TR000522, and National Science Foundation Materials Research Science and Engineering Center grant DMR-1420570.; K.K.P. was sponsored by National Institutes of Health National Center for Advancing Translational Sciences grant 1-UG3-HL-141798-01. S.-J.P. was funded by the Georgia Institute of Technology and Emory University School of Medicine.; This work was performed in part at the Harvard Center for Nanoscale Systems, a member of the National Nanotechnology Infrastructure Network, which is supported by the National Science Foundation under award ECS-0335765. The Center for Nanoscale Systems is part of Harvard University.
• Keywords: TISSUE; CHANNELS; Multidisciplinary Sciences; Science & Technology; PROPAGATION; Science & Technology - Other Topics

Abstract

Biohybrid systems have been developed to better understand the design principles and coordination mechanisms of biological systems. We consider whether two functional regulatory features of the heart-mechanoelectrical signaling and automaticity-could be transferred to a synthetic analog of another fluid transport system: a swimming fish. By leveraging cardiac mechanoelectrical signaling, we recreated reciprocal contraction and relaxation in a muscular bilayer construct where each contraction occurs automatically as a response to the stretching of an antagonistic muscle pair. Further, to entrain this closed-loop actuation cycle, we engineered an electrically autonomous pacing node, which enhanced spontaneous contraction. The biohybrid fish equipped with intrinsic control strategies demonstrated self-sustained body-caudal fin swimming, highlighting the role of feedback mechanisms in muscular pumps such as the heart and muscles.