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Molecular machines stimulate intercellular calcium waves and cause muscle contraction

Nature Nanotechnology volume 18, pages 1051–1059 (2023)Cite this article

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Abstract

Intercellular calcium waves (ICW) are complex signalling phenomena that control many essential biological activities, including smooth muscle contraction, vesicle secretion, gene expression and changes in neuronal excitability. Accordingly, the remote stimulation of ICW could result in versatile biomodulation and therapeutic strategies. Here we demonstrate that light-activated molecular machines (MM)—molecules that perform mechanical work on the molecular scale—can remotely stimulate ICW. MM consist of a polycyclic rotor and stator that rotate around a central alkene when activated with visible light. Live-cell calcium-tracking and pharmacological experiments reveal that MM-induced ICW are driven by the activation of inositol-triphosphate-mediated signalling pathways by unidirectional, fast-rotating MM. Our data suggest that MM-induced ICW can control muscle contraction in vitro in cardiomyocytes and animal behaviour in vivo in Hydra vulgaris. This work demonstrates a strategy for directly controlling cell signalling and downstream biological function using molecular-scale devices.

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Fig. 1: Structures of MM used in this study, their mechanism of rotation and their activation to induce calcium waves in HEK293 cells.
Fig. 2: Mechanistic study of calcium waves induced by MM.
Fig. 3: MM cause localized calcium release, contraction and beating in cardiomyocytes.
Fig. 4: MM induce regional calcium waves in vivo.
Fig. 5: MM induce contraction in H. vulgaris.

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Data availability

All data supporting the findings of this study are available within the article and its supplementary information. Source data are provided with this paper. Additional raw data and analysis code are available via GitHub at https://github.com/jlb48249/MM-ICW.

Code availability

Data analysis scripts are available via GitHub at https://github.com/jlb48249/MM-ICW.

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Acknowledgements

This project received funding from the Discovery Institute, the Robert A. Welch Foundation (C-2017-20190330), the National Science Foundation Graduate Research Fellowship Program (J.L.B.), the DEVCOM Army Research Laboratory under Cooperative Agreement W911NF-18-2-0234 (A.R.v.V.) and the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 843116 (A.L.S.). 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 Army Research Laboratory or the US government. The US government is authorized to reproduce and distribute reprints for government purposes notwithstanding any copyright notation herein. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. This work was conducted in part using resources from the Light Microscopy Facility and the Shared Equipment Authority at Rice University. We acknowledge Z. C. Sanchez (Vanderbilt University) for useful help and advice regarding the growth and activity of cardiomyocytes.

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Authors and Affiliations

  1. Department of Chemistry, Rice University, Houston, TX, USA

    Jacob L. Beckham, Alexis R. van Venrooy, Gang Li, Bowen Li, Dallin Arnold, John T. Li, Ana L. Santos, Gautam Chaudhry & Dongdong Liu

  2. Department of Electrical Engineering, Rice University, Houston, TX, USA

    Soonyoung Kim, Guillaume Duret & Xuan Zhao

  3. IdISBA—Fundación de Investigación Sanitaria de las Islas Baleares, Palma, Spain

    Ana L. Santos

  4. Department of Bioengineering, Department of Electrical Engineering, Rice University, Houston, TX, USA

    Jacob T. Robinson

  5. Department of Chemistry, Smalley-Curl Institute, NanoCarbon Center and Rice Advanced Materials Institute, Department of Materials Science and Nanoengineering, Department of Computer Science, Rice University, Houston, TX, USA

    James M. Tour

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  1. Jacob L. Beckham
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Contributions

Conceptualization: J.L.B., A.R.v.V. and J.M.T. Methodology: J.L.B., G.D., S.K., X.Z. and A.L.S. Organic synthesis: A.R.v.V., G.L., B.L., D.L. and J.M.T. Formal analysis: J.L.B. Investigation: J.L.B., S.K., G.C., D.A. and J.Z. Resources: J.T.R. and J.M.T. Writing (original draft): J.L.B. Writing (reviewing and editing): J.L.B., G.D., S.K., A.L.S., J.T.R. and J.M.T. Software: J.L.B. and J.T.L. Visualization: J.L.B. Supervision: G.D., J.T.R. and J.M.T. Funding acquisition: J.M.T. Project oversight: J.M.T.

Corresponding authors

Correspondence to Jacob T. Robinson or James M. Tour.

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Competing interests

Rice University owns the intellectual property on the use of electromagnetic (light) activation of MM for the stimulation of ICW. Conflicts of interest are managed through regular disclosure to the Rice University Office of Sponsored Projects and Research Compliance. The authors declare no other competing interests.

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Nature Nanotechnology thanks Carson Bruns, Danijela Gregurec and Gabriela Romero Uribe for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–49, Tables 1 and 4 and Discussion.

Reporting Summary

Supplementary Video 1

Animation of the intrinsic reaction coordinate trajectory for the rate-limiting thermal helix inversion step in MM 1.

Supplementary Video 2

Animation of the intrinsic reaction coordinate trajectory for the rate-limiting thermal helix inversion step in MM 2.

Supplementary Video 3

Animation of the intrinsic reaction coordinate trajectory for the rate-limiting thermal helix inversion step in MM 3.

Supplementary Video 4

Animation of the intrinsic reaction coordinate trajectory for the rate-limiting thermal helix inversion step in MM 4.

Supplementary Video 5

Animation of the intrinsic reaction coordinate trajectory for an alternative relaxation pathway in MM 4.

Supplementary Video 6

Time lapse of Fluo-4 fluorescence in cardiomyocytes treated with MM 1 (8 µM) and Fluo-4 and stimulated with 400 nm laser light for 250 ms at an irradiance of 5.1 × 102 W cm–2. The cell on the left is stimulated at 30 s.

Supplementary Video 7

Time lapse of fluorescence images of a cardiomyocyte treated with MM 1 (8 µM) and CellLight Actin-GFP BacMam 2.0 and stimulated with 400 nm laser light for 250 ms at an irradiance of 5.1 × 102 W cm–2. Stimulation was applied at 30 s. The inward movement of the z lines demonstrates localized contraction at the point of stimulation on the release of calcium ions from the SR.

Supplementary Video 8

Time lapse of bright-field images of cardiomyocytes treated with MM 1 (8 µM) and Fluo-4 and stimulated with 400 nm laser light for 250 ms at an irradiance of 5.1 × 102 W cm–2. The cell on the left is stimulated at 30 s.

Supplementary Video 9

Time lapse of fluorescence images of a cardiomyocyte treated with MM 1 (8 µM) and di-8-Anneps (1 µg ml–1) and stimulated with 400 nm laser light for 250 ms at an irradiance of 5.1 × 102 W cm–2. Stimulation was applied at 30 s. The increase in fluorescence of di-8-Anneps during contraction indicates a change in membrane voltage during an action potential.

Supplementary Video 10

Hydra expressing GCaMP7b in epitheliomuscular cells treated with MM 1 (24 µM) and stimulated with 405 nm laser light for 1 s at an irradiance of 9.0 × 102 W cm–2 (protocol I). Stimulation is applied at 10 s. The blue circle shown at 10 s corresponds to the area of stimulation. The trace shown at the bottom of the video corresponds to the intensity of GCaMP7b fluorescence in the area of stimulation across the timescale of the video. The cyan line in the trace represents the time of stimulus presentation, during which no data were collected.

Supplementary Video 11

Hydra expressing GCaMP7b in epitheliomuscular cells treated with DMSO solvent (0.3% v/v) and stimulated with 405 nm laser light for 1 s at an irradiance of 9.0 × 102 W cm–2 (protocol I). Stimulation is applied at 10 s. The blue circle shown at 10 s corresponds to the area of stimulation. The trace shown at the bottom corresponds to the intensity of GCaMP7b fluorescence in the area of stimulation across the timescale of the video. The cyan line in the trace represents the time of stimulus presentation, during which no data were collected.

Supplementary Video 12

Hydra expressing GCaMP7b in epitheliomuscular cells treated with MM 2 (24 µM) and stimulated with 405 nm laser light for 1 s at an irradiance of 6.8 × 102 W cm–2 (protocol I). Stimulation is applied at 10 s at two distinct locations in the Hydra indicated by the yellow and blue circles that appear during stimulation. The traces shown at the bottom of the video correspond to the intensity of GCaMP7b fluorescence in the areas of stimulation across the timescale of the video.

Supplementary Video 13

Hydra expressing GCaMP7b in epitheliomuscular cells treated with MM 2 (24 µM) and stimulated with 405 nm laser light for 2 s at an irradiance of 9.0 × 102 W cm–2. Light was delivered to the oral region of the Hydra (protocol II) at irregular intervals. The yellow circle around the oral region indicates the region to which stimulation was applied. The trace shown at the bottom of the video corresponds to the intensity of GCaMP7b fluorescence in the whole Hydra across the timescale of the video. The vertical yellow lines in the trace mark times during which the stimulus was presented, during which no data were collected. Contractile and electrophysiological responses were observed on each presentation of stimulus.

Supplementary Video 14

Hydra expressing GCaMP7b in epitheliomuscular cells in the absence of MM or light stimulation. The trace shown at the bottom of the video corresponds to the intensity of GCaMP7b fluorescence in the whole Hydra across the timescale of the video.

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Source Data Fig. 4

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Beckham, J.L., van Venrooy, A.R., Kim, S. et al. Molecular machines stimulate intercellular calcium waves and cause muscle contraction. Nat. Nanotechnol. 18, 1051–1059 (2023). https://doi.org/10.1038/s41565-023-01436-w

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