Wu, Di and Baresch, Diego and Cook, Colin and Ma, Zhichao and Duan, Mengtong and Malounda, Dina and Maresca, David and Abundo, Maria P. and Lee, Justin and Shivaei, Shirin and Mittelstein, David R. and Qiu, Tian and Fischer, Peer and Shapiro, Mikhail G. (2023) Biomolecular actuators for genetically selective acoustic manipulation of cells. Science Advances, 9 (8). Art. No. eadd9186. ISSN 2375-2548. PMCID PMC9946353. doi:10.1126/sciadv.add9186. https://resolver.caltech.edu/CaltechAUTHORS:20230223-575177000.2
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Abstract
The ability to physically manipulate specific cells is critical for the fields of biomedicine, synthetic biology, and living materials. Ultrasound has the ability to manipulate cells with high spatiotemporal precision via acoustic radiation force (ARF). However, because most cells have similar acoustic properties, this capability is disconnected from cellular genetic programs. Here, we show that gas vesicles (GVs)—a unique class of gas-filled protein nanostructures—can serve as genetically encodable actuators for selective acoustic manipulation. Because of their lower density and higher compressibility relative to water, GVs experience strong ARF with opposite polarity to most other materials. When expressed inside cells, GVs invert the cells’ acoustic contrast and amplify the magnitude of their ARF, allowing the cells to be selectively manipulated with sound waves based on their genotype. GVs provide a direct link between gene expression and acoustomechanical actuation, opening a paradigm for selective cellular control in a broad range of contexts.
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| Additional Information: | © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY). We thank J. Friend and A. Vasan for helpful discussion, H. Davis for help with fluorescence microscopy, Z. Jin and M. Buss for assistance with bacteria protein expression, A. Farhadi and B. Ling for providing the mammalian cells, G. Ho for assistance with electron microscopy, D. Sawyer for assistance with ultrasound imaging, and X. Ding for contribution to initial experiments. This work was supported by the National Institutes of Health (R01EB018975 and DP1EB033154 to M.G.S.), the Pew Scholarship in the Biomedical Sciences (to M.G.S.), the Packard Fellowship in Science and Engineering (to M.G.S.), and the U.S. Army Institute for Collaborative Biotechnologies (W911NF-19-D-0001 to M.G.S.). D.W. was supported by a Medical Engineering Amgen Fellowship. D.B. was supported by Newton International Fellowships (NF 161508). D.Mar. was supported by the Human Frontiers Science Program Cross-Disciplinary Fellowship. M.P.A. was supported by A*STAR. J.L. was supported by the Paul and Daisy Soros Fellowship and the NIH F30 Fellowship. S.S. was supported by the NSF Graduate Research Fellowship. M.G.S. is an Investigator of the Howard Hughes Medical Institute. Author contributions: D.W., M.G.S., D.B., and D.Mar. conceived the study. D.W. and D.B. designed, planned, and conducted the purified gas vesicle experiments. D.W., C.C., and D.R.M. designed and fabricated the acoustic devices. D.W. and D.Mal. prepared the gas vesicle samples. D.W. designed, planned, and conducted the bacterial cell experiments. D.W., M.D., J.L., and S.S. designed, planned, and conducted the mammalian cell experiments. Z.M. designed the acoustic hologram with input from T.Q. and P.F.. D.Mar. and M.P.A. contributed to experiments. D.W. analyzed the data. D.W. and M.G.S. wrote the manuscript with input from all authors. M.G.S. supervised the research. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Raw data related to the figures are available at https://doi.org/10.22002/yzpvn-3m661. Competing interests: D.W. and M.G.S. are inventors on two patent applications related to this work filed by California Institute of Technology (no. PCT/US2022/080743, filed 1 December 2022, and no. 18/073,102, filed 1 December 2022). The authors declare that they have no other competing interests. | ||||||||||||||||||||||||||||||
| Group: | Tianqiao and Chrissy Chen Institute for Neuroscience | ||||||||||||||||||||||||||||||
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| Issue or Number: | 8 | ||||||||||||||||||||||||||||||
| PubMed Central ID: | PMC9946353 | ||||||||||||||||||||||||||||||
| DOI: | 10.1126/sciadv.add9186 | ||||||||||||||||||||||||||||||
| Record Number: | CaltechAUTHORS:20230223-575177000.2 | ||||||||||||||||||||||||||||||
| Persistent URL: | https://resolver.caltech.edu/CaltechAUTHORS:20230223-575177000.2 | ||||||||||||||||||||||||||||||
| Usage Policy: | No commercial reproduction, distribution, display or performance rights in this work are provided. | ||||||||||||||||||||||||||||||
| ID Code: | 119486 | ||||||||||||||||||||||||||||||
| Collection: | CaltechAUTHORS | ||||||||||||||||||||||||||||||
| Deposited By: | George Porter | ||||||||||||||||||||||||||||||
| Deposited On: | 24 Feb 2023 03:25 | ||||||||||||||||||||||||||||||
| Last Modified: | 24 Feb 2023 19:23 |
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