Biomolecular actuators for genetically selective acoustic manipulation of cells

Author:

Wu Di1ORCID,Baresch Diego2ORCID,Cook Colin1,Ma Zhichao3ORCID,Duan Mengtong4ORCID,Malounda Dina5ORCID,Maresca David5ORCID,Abundo Maria P.5,Lee Justin4ORCID,Shivaei Shirin4ORCID,Mittelstein David R.1ORCID,Qiu Tian6ORCID,Fischer Peer78ORCID,Shapiro Mikhail G.159ORCID

Affiliation:

1. Division of Engineering and Applied Science, California Institute of Technology, Pasadena, CA, USA.

2. University of Bordeaux, CNRS, Bordeaux INP, I2M, UMR 5295, F-33400 Talence, France.

3. Max Planck Institute for Intelligent Systems, Heisenbergstr. 3, 70569 Stuttgart, Germany.

4. Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA.

5. Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, CA, USA.

6. Institute of Physical Chemistry, University of Stuttgart, Pfaffenwaldring 55, 70569 Stuttgart, Germany.

7. Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany.

8. Institute for Molecular Systems Engineering and Advanced Materials, Heidelberg University, INF 225, 69120 Heidelberg, Germany.

9. Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA, USA.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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