Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Harmonic acoustics for dynamic and selective particle manipulation

Nature Materials volume 21, pages 540–546 (2022)Cite this article

Subjects

Abstract

Precise and selective manipulation of colloids and biological cells has long been motivated by applications in materials science, physics and the life sciences. Here we introduce our harmonic acoustics for a non-contact, dynamic, selective (HANDS) particle manipulation platform, which enables the reversible assembly of colloidal crystals or cells via the modulation of acoustic trapping positions with subwavelength resolution. We compose Fourier-synthesized harmonic waves to create soft acoustic lattices and colloidal crystals without using surface treatment or modifying their material properties. We have achieved active control of the lattice constant to dynamically modulate the interparticle distance in a high-throughput (>100 pairs), precise, selective and reversible manner. Furthermore, we apply this HANDS platform to quantify the intercellular adhesion forces among various cancer cell lines. Our biocompatible HANDS platform provides a highly versatile particle manipulation method that can handle soft matter and measure the interaction forces between living cells with high sensitivity.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Fourier synthesis of harmonic acoustic waves of HANDS to create soft flexible lattices for colloidal crystals or cell–cell pairing and separation.
Fig. 2: Creation of colloid crystal monolayers with cluster and spin dynamics studies via HANDS manipulation.
Fig. 3: HANDS for manipulation of soft matter and living cells for precision quantitative measurements.
Fig. 4: Reversible cell–cell pairings via HANDS for the quantification of intercellular adhesion strength in different cell lines.

Similar content being viewed by others

Data availability

All the data supporting the findings of this study are available in the article and its Supplementary Information. Further information is available from the corresponding author on reasonable request.

Code availability

The acoustic wave simulations were performed with commercial software MATLAB. Computation details can be made available from the corresponding authors on request.

References

  1. Li, B., Zhou, D. & Han, Y. Assembly and phase transitions of colloidal crystals. Nat. Rev. Mater. 1, 15011 (2016).

    Article  CAS  Google Scholar 

  2. Hou, J., Li, M. & Song, Y. Recent advances in colloidal photonic crystal sensors: materials, structures and analysis methods. Nano Today 22, 132–144 (2018).

    Article  CAS  Google Scholar 

  3. Lim, M. X., Souslov, A., Vitelli, V. & Jaeger, H. M. Cluster formation by acoustic forces and active fluctuations in levitated granular matter. Nat. Phys. 15, 460–464 (2019).

    Article  CAS  Google Scholar 

  4. Ozcelik, A. et al. Acoustic tweezers for the life sciences. Nat. Methods 15, 1021–1028 (2018).

    Article  CAS  Google Scholar 

  5. Guo, J. et al. Modular assembly of superstructures from polyphenol-functionalized building blocks. Nat. Nanotechnol. 11, 1105–1111 (2016).

    Article  CAS  Google Scholar 

  6. Manoharan, V. N. Colloidal matter: packing, geometry, and entropy. Science 349, 1253751 (2015).

    Article  Google Scholar 

  7. Aubret, A., Youssef, M., Sacanna, S. & Palacci, J. Targeted assembly and synchronization of self-spinning microgears. Nat. Phys. 14, 1114–1118 (2018).

    Article  CAS  Google Scholar 

  8. Liu, B. et al. Switching plastic crystals of colloidal rods with electric fields. Nat. Commun. 5, 3092 (2014).

    Article  Google Scholar 

  9. Demirors, A. F., Pillai, P. P., Kowalczyk, B. & Grzybowski, B. A. Colloidal assembly directed by virtual magnetic moulds. Nature 503, 99–103 (2013).

    Article  Google Scholar 

  10. Yang, D., Ye, S. & Ge, J. Solvent wrapped metastable colloidal crystals: highly mutable colloidal assemblies sensitive to weak external disturbance. J. Am. Chem. Soc. 135, 18370–18376 (2013).

    Article  CAS  Google Scholar 

  11. Ashkin, A., Dziedzic, J. M. & Yamane, T. Optical trapping and manipulation of single cells using infrared laser beams. Nature 330, 769–771 (1987).

    Article  CAS  Google Scholar 

  12. Guo, F. et al. Controlling cell-cell interactions using surface acoustic waves. Proc. Natl Acad. Sci. USA 112, 43–48 (2015).

    Article  CAS  Google Scholar 

  13. Collins, D. J. et al. Two-dimensional single-cell patterning with one cell per well driven by surface acoustic waves. Nat. Commun. 6, 8686 (2015).

    Article  CAS  Google Scholar 

  14. Sitters, G. et al. Acoustic force spectroscopy. Nat. Methods 12, 47–50 (2015).

    Article  CAS  Google Scholar 

  15. Kamsma, D. et al. Single-cell acoustic force spectroscopy: resolving kinetics and strength of T cell adhesion to fibronectin. Cell Rep. 24, 3008–3016 (2018).

    Article  CAS  Google Scholar 

  16. Marzo, A. & Drinkwater, B. W. Holographic acoustic tweezers. Proc. Natl Acad. Sci. USA 116, 84–89 (2019).

    Article  CAS  Google Scholar 

  17. Melde, K., Mark, A. G., Qiu, T. & Fischer, P. Holograms for acoustics. Nature 537, 518–522 (2016).

    Article  CAS  Google Scholar 

  18. Hirayama, R., Plasencia, D. M., Masuda, N. & Subramanian, S. A volumetric display for visual, tactile and audio presentation using acoustic trapping. Nature 575, 320–323 (2019).

    Article  CAS  Google Scholar 

  19. Tian, Z. et al. Wave number–spiral acoustic tweezers for dynamic and reconfigurable manipulation of particles and cells. Sci. Adv. 5, eaau6062 (2019).

    Article  CAS  Google Scholar 

  20. Baudoin, M. et al. Folding a focalized acoustical vortex on a flat holographic transducer: miniaturized selective acoustical tweezers. Sci. Adv. 5, eaav1967 (2019).

    Article  CAS  Google Scholar 

  21. Friend, J. R. & Yeo, L. Y. Microscale acoustofluidics: Microfluidics driven via acoustics and ultrasonics. Rev. Mod. Phys. 83, 647–704 (2011).

    Article  Google Scholar 

  22. Huang, P. H. et al. Acoustofluidic synthesis of particulate nanomaterials. Adv. Sci. 6, 1900913 (2019).

    Article  CAS  Google Scholar 

  23. Gu, Y. et al. Acoustofluidic centrifuge for nanoparticle enrichment and separation. Sci. Adv. 7, eabc0467 (2021).

    Article  CAS  Google Scholar 

  24. Fan, X.-D., Zou, Z. & Zhang, L. Acoustic vortices in inhomogeneous media. Phys. Rev. Res. 1, 032014 (2019).

    Article  CAS  Google Scholar 

  25. Delsing, P. et al. The 2019 surface acoustic waves roadmap. J. Phys. D 52, 353001 (2019).

    Article  CAS  Google Scholar 

  26. Schuetz, M. J. et al. Acoustic traps and lattices for electrons in semiconductors. Phys. Rev. X 7, 041019 (2017).

    Google Scholar 

  27. Schülein, F. J. et al. Fourier synthesis of radiofrequency nanomechanical pulses with different shapes. Nat. Nanotechnol. 10, 512–516 (2015).

    Article  Google Scholar 

  28. Weiß, M. et al. Optomechanical wave mixing by a single quantum dot. Optica 8, 291–300 (2021).

    Article  Google Scholar 

  29. Hosseini, B. H. et al. Immune synapse formation determines interaction forces between T cells and antigen-presenting cells measured by atomic force microscopy. Proc. Natl Acad. Sci. USA 106, 17852–17857 (2009).

    Article  CAS  Google Scholar 

  30. Liu, B., Chen, W., Evavold, B. D. & Zhu, C. Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling. Cell 157, 357–368 (2014).

    Article  CAS  Google Scholar 

  31. Dholakia, K. & Reece, P. Optical micromanipulation takes hold. Nano Today 1, 18–27 (2006).

    Article  Google Scholar 

  32. Feng, Y. et al. Mechanosensing drives acuity of αβ T-cell recognition. Proc. Natl Acad. Sci. USA 114, E8204–E8213 (2017).

    Article  CAS  Google Scholar 

  33. Chen, S. & Lee, L. P. Non-invasive microfluidic gap junction assay. Integr. Biol. 2, 130–138 (2010).

    Article  CAS  Google Scholar 

  34. Glynne-Jones, P., Boltryk, R. J., Harris, N. R., Cranny, A. W. & Hill, M. Mode-switching: a new technique for electronically varying the agglomeration position in an acoustic particle manipulator. Ultrasonics 50, 68–75 (2010).

    Article  CAS  Google Scholar 

  35. Marzo, A., Caleap, M. & Drinkwater, B. W. Acoustic virtual vortices with tunable orbital angular momentum for trapping of mie particles. Phys. Rev. Lett. 120, 044301 (2018).

    Article  CAS  Google Scholar 

  36. Auwerx, J. The human leukemia cell line, THP-1: a multifacetted model for the study of monocyte-macrophage differentiation. Experientia 47, 22–31 (1991).

    Article  CAS  Google Scholar 

  37. Chu, Y. S. et al. Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J. Cell Biol. 167, 1183–1194 (2004).

    Article  CAS  Google Scholar 

  38. Casella, J. F., Flanagan, M. D. & Lin, S. Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293, 302–305 (1981).

    Article  CAS  Google Scholar 

  39. Kang, J. H. et al. Noninvasive monitoring of single-cell mechanics by acoustic scattering. Nat. Methods 16, 263–269 (2019).

    Article  CAS  Google Scholar 

  40. Palmer, C. P. et al. Single cell adhesion measuring apparatus (SCAMA): application to cancer cell lines of different metastatic potential and voltage-gated Na+ channel expression. Eur. Biophys. J. 37, 359–368 (2008).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge support from the Shared Materials Instrumentation Facility at Duke University. We thank S. Suresh, M. Dao, Z. Mao and J. Rich for their critical feedback and helpful discussions. We acknowledge support from the National Institutes of Health (grant numbers R01GM141055 (T.J.H.), R01GM132603 (T.J.H.), U18TR003778 (T.J.H.) and UH3TR002978 (T.J.H.)) and the National Science Foundation (grant numbers ECCS-1807601 (T.J.H.) and CMMI-2104295 (T.J.H.)).

Author information

Authors and Affiliations

  1. Thomas Lord Department of Mechanical Engineering and Materials Science, Duke University, Durham, NC, USA

    Shujie Yang, Zhenhua Tian, Zeyu Wang, Joseph Rufo, Jianping Xia, Hunter Bachman, Po-Hsun Huang, Mengxi Wu, Chuyi Chen & Tony Jun Huang

  2. C. Eugene Bennett Department of Chemistry, West Virginia University, Morgantown, WV, USA

    Peng Li

  3. Alfred E. Mann Institute for Biomedical Engineering, University of Southern California, Los Angeles, CA, USA

    John Mai

  4. Renal Division and Division of Engineering in Medicine, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Luke P. Lee

  5. Department of Bioengineering, Department of Electrical Engineering and Computer Science, University of California at Berkeley, Berkeley, CA, USA

    Luke P. Lee

  6. Institute of Quantum Biophysics, Department of Biophysics, Sungkyunkwan University, Suwon, Korea

    Luke P. Lee

Authors
  1. Shujie Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenhua Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zeyu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joseph Rufo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John Mai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianping Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hunter Bachman
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Po-Hsun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mengxi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chuyi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Luke P. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Tony Jun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.Y. conceived the idea. S.Y., Z.T., P.L., L.P.L. and T.J.H. designed the research. S.Y. performed the research. Z.W. performed the western blot analysis. S.Y., J.X. and C.C. did the simulation. S.Y., Z.W., Z.T., H.B., C.C., P.L., P.-H.H., M.W., L.P.L. and T.J.H. analysed data. S.Y., P.-H.H., H.B., Z.T. and L.P.L. drew the figures. S.Y., Z.T., Z.W., H.B., P.L., P.-H.H., J.R., J.M., L.P.L. and T.J.H. wrote the paper. S.Y., Z.T., J.R., H.B., P.L., J.M., L.P.L. and T.J.H. revised the paper.

Corresponding authors

Correspondence to Luke P. Lee or Tony Jun Huang.

Ethics declarations

Competing interests

T.J.H. has cofounded a start-up company, Ascent Bio-Nano Technologies Inc., to commercialize technologies involving acoustofluidics and acoustic tweezers. The remaining authors declare no competing interests.

Peer review

Peer review information

Nature Materials thanks Hubert Krenner, Adrian Neild and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Notes 1–8, Figs. 1–6 and Table 1.

Supplementary Video 1

Selective and reversible pairing of two cells (U937) by the HANDS platform while keeping neighbouring cells intact.

Supplementary Video 2

Creation of colloidal crystal from a cluster by the HANDS platform.

Supplementary Video 3

Controls of rotational direction and spinning of a colloidal crystal monolayer by the HANDS platform.

Supplementary Video 4

Different crystal configurations of colloidal monolayers with varied spin speeds (with particle number n = 6) by the HANDS platform.

Supplementary Video 5

Reconfiguration of acoustic wells for single-colloid trapping and pairing by the HANDS platform: connected acoustic wells and isolated acoustic wells.

Supplementary Video 6

Demonstration of the repeatable and reversible pairing of single particles by the HANDS platform.

Supplementary Video 7

High-throughput pairing for colloidal particles and cells by the HANDS platform.

Supplementary Video 8

Reversible pairing of living cells (U937) in the x and y directions by the HANDS platform.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, S., Tian, Z., Wang, Z. et al. Harmonic acoustics for dynamic and selective particle manipulation. Nat. Mater. 21, 540–546 (2022). https://doi.org/10.1038/s41563-022-01210-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41563-022-01210-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing