Skip to main content
Log in

Magnetically actuated microstructured surfaces can actively modify cell migration behaviour

  • Published:
Biomedical Microdevices Aims and scope Submit manuscript

Abstract

We present a study on the application of magnetically actuated polymer micropillar surfaces in modifying the migration behaviour of cells. We show that micropillar surfaces actuated at a frequency of 1 Hz can cause more than a 5-fold decrease in cell migration rates compared to controls, whereas non-actuated micropillar surfaces cause no statistically significant alterations in cell migration rates. The effectiveness of the micropillar arrays in impeding cell migration depends on micropillar density and placement patterns, as well as the direction of micropillar actuation with respect to the direction of cell migration. Since the magnetic micropillar surfaces presented can be actuated remotely with small external magnetic fields, their integration with implants could provide new possibilities for in-vivo tissue engineering applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • C. Moraes, C. A. Simmons, Y. Sun, Cell mechanics meets MEMS. Canadian Society ofMechanical Engineers Fall 2006 Bulletin. http://cmed.lab.mcgill.ca/wp-content/uploads/2015/08/OC1_CSMEBulletin-CellMechanics_MEMS.pdf

  • C. Moraes, J. Chen, Y. Sun, C. A. Simmons, Microfabricated arrays for high-throughput screening of cellular response to cyclic substrate deformation. Lab Chip. 10(2), 227–234 (2010)

    Article  Google Scholar 

  • D. Desmaële, M. Boukallel, S. Régnier, Actuation means for the mechanical stimulation of living cells via microelectromechanical systems: a critical review. J. Biomech. 44(8), 1433–1446 (2011)

    Article  Google Scholar 

  • Akbari S, Niklaus M, Shea H. Arrays of EAP micro-actuators for single-cell stretching applications.. 2010:76420 H-76420 H-10.

  • F. Zhang, S. Anderson, X. Zheng, et al., Cell force mapping using a double-sided micropillar array based on the moiré fringe method. Appl. Phys. Lett. 105(3), 033702 (2014)

    Article  Google Scholar 

  • L. E. Dickinson, D. R. Rand, J. Tsao, W. Eberle, S. Gerecht, Endothelial cell responses to micropillar substrates of varying dimensions and stiffness. J. Biomed. Mater. Res. A. 100(6), 1457–1466 (2012)

    Article  Google Scholar 

  • S. Ghassemi, G. Meacci, S. Liu, et al., Cells test substrate rigidity by local contractions on submicrometer pillars. Proc. Natl. Acad. Sci. U. S. A. 109(14), 5328–5333 (2012)

    Article  Google Scholar 

  • Z. Pan, C. Yan, R. Peng, Y. Zhao, Y. He, J. Ding, Control of cell nucleus shapes via micropillar patterns. Biomaterials 33(6), 1730–1735 (2012)

    Article  Google Scholar 

  • J. le Digabel, N. Biais, J. Fresnais, J. F. Berret, P. Hersen, B. Ladoux, Magnetic micropillars as a tool to govern substrate deformations. Lab Chip 11, 2630–2636 (2011)

    Article  Google Scholar 

  • I. Schoen, W. Hu, E. Klotzsch, V. Vogel, Probing cellular traction forces by micropillar arrays: contribution of substrate warping to pillar deflection. Nano Letters. 10(5), 1823–1830 (2010)

    Article  Google Scholar 

  • S. Ghassemi, N. Biais, K. Maniura, S. J. Wind, M. P. Sheetz, J. Hone, Fabrication of elastomer pillar arrays with modulated stiffness for cellular force measurements. J. Vac. Sci. Technol. B: Microelectron. Nanometer Struct. 26(6), 2549–2553 (2009a)

    Article  Google Scholar 

  • S. Ghassemi, O. Rossier, M. P. Sheetz, S. J. Wind, J. Hone, Gold-tipped elastomeric pillars for cellular mechanotransduction. J Vac. Sci. Technol. B: Microelectron. Nanometer Struct. 27, 3088 (2009b)

    Article  Google Scholar 

  • N. J. Sniadecki, A. Anguelouch, M. T. Yang, et al., Magnetic microposts as an approach to apply forces to living cells. Proc. Natl. Acad. Sci. 104(37), 14553 (2007)

    Article  Google Scholar 

  • N. J. Sniadecki, C. M. Lamb, Y. Liu, C. S. Chen, D. H. Reich, Magnetic microposts for mechanical stimulation of biological cells: fabrication, characterization, and analysis. Rev Sci Instrum. 79, 044302 (2008)

    Article  Google Scholar 

  • J. Fu, Y. K. Wang, M. T. Yang, et al., Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Methods. 7(9), 733–736 (2010)

    Article  Google Scholar 

  • M. Ghibaudo, J. Di Meglio, P. Hersen, B. Ladoux, Mechanics of cell spreading within 3D-micropatterned environments. Lab Chip 11(5), 805–812 (2011)

    Article  Google Scholar 

  • N. Tymchenko, J. Wallentin, S. Petronis, L. Bjursten, B. Kasemo, J. Gold, A novel cell force sensor for quantification of traction during cell spreading and contact guidance. Biophys. J. 93(1), 335–345 (2007)

    Article  Google Scholar 

  • M. T. Yang, N. J. Sniadecki, C. S. Chen, Geometric considerations of micro-to nanoscale elastomeric post arrays to study cellular traction forces. Adv. Mater. 19(20), 3119–3123 (2007)

    Article  Google Scholar 

  • A. Buxboim, D. E. Discher, Stem cells feel the difference. Nat. Methods. 7(9), 695 (2010)

    Article  Google Scholar 

  • Y. Zhu, D. S. Antao, R. Xiao, E. N. Wang, Real-time manipulation with magnetically tunable structures. Adv. Mater. 26(37), 6442–6446 (2014)

    Article  Google Scholar 

  • F. Khademolhosseini, M. Chiao, Fabrication and patterning of magnetic polymer micropillar structures using a dry-nanoparticle embedding technique. J. Microelectromech. Syst. 22(1), 131–139 (2013)

    Article  Google Scholar 

  • Y. C. Yung, H. Vandenburgh, D. J. Mooney, Cellular strain assessment tool (CSAT): precision-controlled cyclic uniaxial tensile loading. J. Biomech. 42(2), 178–182 (2009a)

    Article  Google Scholar 

  • J. H. C. Wang, P. Goldschmidt-Clermont, J. Wille, F. C. P. Yin, Specificity of endothelial cell reorientation in response to cyclic mechanical stretching. J. Biomech. 34(12), 1563–1572 (2001)

    Article  Google Scholar 

  • S. Jungbauer, H. Gao, J. P. Spatz, R. Kemkemer, Two characteristic regimes in frequency-dependent dynamic reorientation of fibroblasts on cyclically stretched substrates. Biophys. J. 95(7), 3470–3478 (2008)

    Article  Google Scholar 

  • L. M. Crosby, C. Luellen, Z. Zhang, L. L. Tague, S. E. Sinclair, C. M. Waters, Balance of life and death in alveolar epithelial type II cells: proliferation, apoptosis, and the effects of cyclic stretch on wound healing. Am. J. Physiol. Lung Cell Mol. Physiol. 301(4), L536–L546 (2011)

    Article  Google Scholar 

  • S. Saika, L. Werner, F. J. Lovicu, Lens epithelium and posterior capsular opacification (Tokyo, Springer Japan KK, 2014)

    Book  Google Scholar 

  • F. N. Pirmoradi, J. K. Jackson, H. M. Burt, M. Chiao, On-demand controlled release of docetaxel from a battery-less MEMS drug delivery device. Lab Chip 11(16), 2744–2752 (2011)

    Article  Google Scholar 

  • R. Riahi, Y. Yang, D. D. Zhang, P. K. Wong, Advances in wound-healing assays for probing collective cell migration. J Lab Autom. 17(1), 59–65 (2012)

    Article  Google Scholar 

  • R. van Horssen, T. L. ten Hagen, Crossing barriers: the new dimension of 2D cell migration assays. J. Cell. Physiol. 226(1), 288–290 (2011)

    Article  Google Scholar 

  • P. Vitorino, T. Meyer, Modular control of endothelial sheet migration. Genes Dev. 22(23), 3268–3281 (2008)

    Article  Google Scholar 

  • Y. C. Yung, J. Chae, M. J. Buehler, C. P. Hunter, D. J. Mooney, Cyclic tensile strain triggers a sequence of autocrine and paracrine signaling to regulate angiogenic sprouting in human vascular cells. Proc. Natl. Acad. Sci. 106(36), 15279–15284 (2009b)

    Article  Google Scholar 

  • E. Fong, S. Tzlil, D. A. Tirrell, Boundary crossing in epithelial wound healing. Proc. Natl. Acad. Sci. U. S. A. 107(45), 19302–19307 (2010)

    Article  Google Scholar 

  • P. J. Sammak, L. E. Hinman, P. O. Tran, M. D. Sjaastad, T. E. Machen, How do injured cells communicate with the surviving cell monolayer? J. Cell Sci. 110(4), 465–475 (1997)

    Google Scholar 

  • M. Poujade, E. Grasland-Mongrain, A. Hertzog, et al., Collective migration of an epithelial monolayer in response to a model wound. Proc. Natl. Acad. Sci. U. S. A. 104(41), 15988–15993 (2007)

    Article  Google Scholar 

  • E. R. Block, A. R. Matela, N. SundarRaj, E. R. Iszkula, J. K. Klarlund, Wounding induces motility in sheets of corneal epithelial cells through loss of spatial constraints: role of heparin-binding epidermal growth factor-like growth factor signaling. J. Biol Chem. 279(23), 24307–24312 (2004)

    Article  Google Scholar 

  • C. W. Wolgemuth, Lamellipodial contractions during crawling and spreading. Biophys. J. 89(3), 1643–1649 (2005)

    Article  Google Scholar 

  • M. A. Schwartz, A. R. Horwitz, Integrating adhesion, protrusion, and contraction during cell migration. Cell 125(7), 1223–1225 (2006)

    Article  Google Scholar 

  • N. D. Gallant, K. E. Michael, A. J. Garcia, Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol. Biol. Cell 16(9), 4329–4340 (2005)

    Article  Google Scholar 

  • L. Lamalice, F. Le Boeuf, J. Huot, Endothelial cell migration during angiogenesis. Circ. Res. 100(6), 782–794 (2007)

    Article  Google Scholar 

  • R. J. Petrie, A. D. Doyle, K. M. Yamada, Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 10(8), 538–549 (2009)

    Article  Google Scholar 

  • Dartsch P, Hämmerle H, Betz E. Orientation of cultured arterial smooth muscle cells growing on cyclically stretched substrates. Cells Tissues Organs (Print). 1986; 125(2):108–113.

  • P. Dartsch, E. Betz, Response of cultured endothelial cells to mechanical stimulation. Basic Res. Cardiol. 84(3), 268–281 (1989)

    Article  Google Scholar 

Download references

Acknowledgment

This project was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants to M. Chiao and C.J. Lim. Fabrication was partly funded by CMC Microsystems. F. Khademolhosseini was funded by the NSERC Vanier Canada Graduate Scholarship and fellowships from the Izaak Walton Killam Foundation and The University of British Columbia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Khademolhosseini.

Electronic supplementary material

ESM 1

(DOCX 2888 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khademolhosseini, F., Liu, CC., Lim, C.J. et al. Magnetically actuated microstructured surfaces can actively modify cell migration behaviour. Biomed Microdevices 18, 13 (2016). https://doi.org/10.1007/s10544-016-0033-7

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s10544-016-0033-7

Keywords

Navigation