Skip to main content
SpringerLink
Log in

Recent advances in biological uses of traction force microscopy

  • Published:
International Journal of Precision Engineering and Manufacturing Aims and scope Submit manuscript

Abstract

Cell traction forces (CTF) generated by the actomyosin cytoskeleton onto a substrate or extracellular matrix (ECM) are essential for many biological processes, including developmental morphogenesis, tissue homeostasis, and cancer metastasis. Because the cellular physical properties are closely related to the pathological states of the cells, affected by various physicochemical stimuli from their neighboring cells or surrounding environments, it is crucial to develop a quantitative measure for cellular responses to these external stimuli. Since the pioneering work of Harris et al. in 1980s1, traction force microscopy (TFM) has been widely used as a standard tool that allows the optical measurement of cellular tractions exerted on 2- and 3-dimensional soft elastic substrates. Recently, there have been many technical advances in conventional TFM to enhance its spatial and temporal resolutions as well as the range of applicability. In this review, we provide a survey on the recent advancement in TFM, especially with a special emphasis on platforms that can externally apply various stimuli such as fluid shear, mechanical tension or compression, biochemical factors, and electric field in a physiologically relevant regime.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

TFM:

traction force microscopy

CTF:

cell traction force

ECM:

extracellular matrix

FAs:

focal adhesions

ECs:

endothelial cells

EF:

electric field

PA:

polyacrylamide

τ:

shear stress

PDMS:

polydimethylsiloxane

HA:

hyaluronic acid

PEGDA:

poly (ethylene glycol) diacrylate

References

  1. Harris, A. K., Wild, P., and Stopak, D., “Silicone Rubber Substrata: A New Wrinkle in the Study of Cell Locomotion,” Science, Vol. 208, No. 4440, pp. 177–179, 1980.

    Article  Google Scholar 

  2. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M., and Ingber, D. E., “Geometric Control of Cell Life and Death,” Science, Vol. 276, No. 5317, pp. 1425–1428, 1997.

    Article  Google Scholar 

  3. Meredith, J. E., Fazeli, B., and Schwartz, M. A., “The Extracellular Matrix as a Cell Survival Factor,” Molecular Biology of the Cell, Vol. 4, No. 9, pp. 953–961, 1993.

    Article  Google Scholar 

  4. Murrell, M., Oakes, P. W., Lenz, M., and Gardel, M. L., “Forcing Cells into Shape: The Mechanics of Actomyosin Contractility,” Nature Reviews Molecular Cell Biology, Vol. 16, No. 8, pp. 486–498, 2015.

    Article  Google Scholar 

  5. Pelham, R. J. and Wang, Y.-l., “Cell Locomotion and Focal Adhesions are Regulated by Substrate Flexibility,” Proceedings of the National Academy of Sciences, Vol. 94, No. 25, pp. 13661–13665, 1997.

    Article  Google Scholar 

  6. Sheetz, M. P., Felsenfeld, D. P., and Galbraith, C. G., “Cell Migration: Regulation of Force on Extracellular-Matrix-Integrin Complexes,” Trends in Cell Biology, Vol. 8, No. 2, pp. 51–54, 1998.

    Article  Google Scholar 

  7. Aratyn-Schaus, Y. and Gardel, M. L., “Transient Frictional Slip between Integrin and the ECM in Focal Adhesions Under Myosin II Tension,” Current Biology, Vol. 20, No. 13, pp. 1145–1153, 2010.

    Article  Google Scholar 

  8. Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., et al., “Force and Focal Adhesion Assembly: A Close Relationship Studied using Elastic Micropatterned Substrates,” Nature Cell Biology, Vol. 3, No. 5, pp. 466–472, 2001.

    Article  Google Scholar 

  9. Gardel, M. L., Schneider, I. C., Aratyn-Schaus, Y., and Waterman, C. M., “Mechanical Integration of Actin and Adhesion Dynamics in Cell Migration,” Annual Review of Cell and Developmental Biology, Vol. 26, No. pp. 315, 2010.

    Article  Google Scholar 

  10. Burton, K. and Taylor, D. L., “Traction Forces of Cytokinesis Measured with Optically Modified Elastic Substrata,” Nature, Vol. 385, No. 6615, pp. 450–454, 1997.

    Article  Google Scholar 

  11. Harris, A. K., Stopak, D., and Wild, P., “Fibroblast Traction as a Mechanism for Collagen Morphogenesis,” Nature, Vol. 290, No. 5803, pp. 249–251, 1981.

    Article  Google Scholar 

  12. Lee, J., Leonard, M., Oliver, T., Ishihara, A., and Jacobson, K., “Traction Forces Generated by Locomoting Keratocytes,” The Journal of Cell Biology, Vol. 127, No. 6, pp. 1957–1964, 1994.

    Article  Google Scholar 

  13. Butler, J. P., Tolic-Nørrelykke, I. M., Fabry, B., and Fredberg, J. J., “Traction Fields, Moments, and Strain Energy that Cells Exert on their Surroundings,” American Journal of Physiology-Cell Physiology, Vol. 282, No. 3, pp. C595–C605, 2002.

    Article  Google Scholar 

  14. Sabass, B., Gardel, M. L., Waterman, C. M., and Schwarz, U. S., “High Resolution Traction Force Microscopy based on Experimental and Computational Advances,” Biophysical Journal, Vol. 94, No. 1, pp. 207–220, 2008.

    Article  Google Scholar 

  15. Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K., and Chen, C. S., “Cells Lying on a Bed of Microneedles: An Approach to Isolate Mechanical Force,” Proceedings of the National Academy of Sciences, Vol. 100, No. 4, pp. 1484–1489, 2003.

    Article  Google Scholar 

  16. Tolic-Nørrelykke, I. M., Butler, J. P., Chen, J., and Wang, N., “Spatial and Temporal Traction Response in Human Airway Smooth Muscle Cells,” American Journal of Physiology-Cell Physiology, Vol. 283, No. 4, pp. C1254–C1266, 2002.

    Article  Google Scholar 

  17. Franck, C., Hong, S., Maskarinec, S. A., Tirrell, D. A., and Ravichandran, G., “Three-Dimensional Full-Field Measurements of Large Deformations in Soft Materials using Confocal Microscopy and Digital Volume Correlation,” Experimental Mechanics, Vol. 47, No. 3, pp. 427–438, 2007.

    Article  Google Scholar 

  18. Legant, W. R., Miller, J. S., Blakely, B. L., Cohen, D. M., Genin, G. M., and Chen, C. S., “Measurement of Mechanical Tractions Exerted by Cells in Three-Dimensional Matrices,” Nature Methods, Vol. 7, No. 12, pp. 969–971, 2010.

    Article  Google Scholar 

  19. Jin, S., Kim, J. H., and Yun, W.-S., “Development of Dynamic Well Plate System for Cell Culture with Mechanical Stimulus of Shear Stress And Magnetic Field,” Int. J. Precis. Eng. Manuf., Vol. 16, No. 10, pp. 2235–2239, 2015.

    Article  Google Scholar 

  20. Jo, H. and Shin, J. H., “Special Issue on Mechanobiology and Diseases, Biomedical Engineering Letters, Vol. 5, No. 3, pp. 159–161, 2015.

    Article  Google Scholar 

  21. Geiger, B., Spatz, J. P., and Bershadsky, A. D., “Environmental Sensing through Focal Adhesions,” Nature Reviews Molecular Cell Biology, Vol. 10, No. 1, pp. 21–33, 2009.

    Article  Google Scholar 

  22. McCain, M. L., Lee, H., Aratyn-Schaus, Y., Kléber, A. G., and Parker, K. K., “Cooperative Coupling of Cell-Matrix and Cell–Cell Adhesions in Cardiac Muscle,” Proceedings of the National Academy of Sciences, Vol. 109, No. 25, pp. 9881–9886, 2012.

    Article  Google Scholar 

  23. Davies, P. F., “Flow-Mediated Endothelial Mechanotransduction,” Physiological Reviews, Vol. 75, No. 3, pp. 519–560, 1995.

    Google Scholar 

  24. Park, C. Y., Zhou, E. H., Tambe, D., Chen, B., Lavoie, T., et al., “High-Throughput Screening for Modulators of Cellular Contractile Force,” Integrative Biology, Vol. 7, No. 10, pp. 1318–1324, 2015.

    Article  Google Scholar 

  25. Malek, A. M., Alper, S. L., and Izumo, S., “Hemodynamic Shear Stress and Its Role in Atherosclerosis,” JAMA, Vol. 282, No. 21, pp. 2035–2042, 1999.

    Article  Google Scholar 

  26. Park, J. Y., White, J. B., Walker, N., Kuo, C.-H., Cha, W., et al., “Responses of Endothelial Cells to Extremely Slow Flows,” Biomicrofluidics, Vol. 5, No. 2, Paper No. 22211, 2011.

    Article  Google Scholar 

  27. Song, J. W. and Munn, L. L., “Fluid Forces Control Endothelial Sprouting,” Proceedings of the National Academy of Sciences, Vol. 108, No. 37, pp. 15342–15347, 2011.

    Article  Google Scholar 

  28. Ng, J., Shin, Y., and Chung, S., “Microfluidic Platforms for the Study of Cancer Metastasis, Biomedical Engineering Letters, Vol. 2, No. 2, pp. 72–77, 2012.

    Article  Google Scholar 

  29. Conway, D. E., Breckenridge, M. T., Hinde, E., Gratton, E., Chen, C. S., and Schwartz, M. A., “Fluid Shear Stress on Endothelial Cells Modulates Mechanical Tension Across VE-Cadherin and PECAM-1,” Current Biology, Vol. 23, No. 11, pp. 1024–1030, 2013.

    Article  Google Scholar 

  30. Hur, S. S., Del Alamo, J. C., Park, J. S., Li, Y.-S., Nguyen, H. A., et al., “Roles of Cell Confluency and Fluid Shear in 3-Dimensional Intracellular Forces in Endothelial Cells,” Proceedings of the National Academy of Sciences, Vol. 109, No. 28, pp. 11110–11115, 2012.

    Article  Google Scholar 

  31. Steward, R., Tambe, D., Hardin, C. C., Krishnan, R., and Fredberg, J. J., “Fluid Shear, Intercellular Stress, and Endothelial Cell Alignment,” American Journal of Physiology-Cell Physiology, Vol. 308, No. 8, pp. C657–C664, 2015.

    Article  Google Scholar 

  32. Ting, L. H., Jahn, J. R., Jung, J. I., Shuman, B. R., Feghhi, S., et al., “Flow Mechanotransduction Regulates Traction Forces, Intercellular Forces, and Adherens Junctions,” American Journal of Physiology-Heart and Circulatory Physiology, Vol. 302, No. 11, pp. H2220–H2229, 2012.

    Article  Google Scholar 

  33. Perrault, C. M., Brugues, A., Bazellieres, E., Ricco, P., Lacroix, D., and Trepat, X., “Traction Forces of Endothelial Cells under Slow Shear Flow,” Biophysical Journal, Vol. 109, No. 8, pp. 1533–1536, 2015.

    Article  Google Scholar 

  34. Lam, R. H., Sun, Y., Chen, W., and Fu, J., “Elastomeric Microposts Integrated into Microfluidics for Flow-Mediated Endothelial Mechanotransduction Analysis,” Lab on a Chip, Vol. 12, No. 10, pp. 1865–1873, 2012.

    Article  Google Scholar 

  35. Shiu, Y.-T., Li, S., Marganski, W. A., Usami, S., Schwartz, M. A., et al., “Rho Mediates the Shear-Enhancement of Endothelial Cell Migration and Traction Force Generation,” Biophysical Journal, Vol. 86, No. 4, pp. 2558–2565, 2004.

    Article  Google Scholar 

  36. Discher, D. E., Janmey, P., and Wang, Y.-l., “Tissue Cells Feel and Respond to the Stiffness of their Substrate,” Science, Vol. 310, No. 5751, pp. 1139–1143, 2005.

    Article  Google Scholar 

  37. Palchesko, R. N., Zhang, L., Sun, Y., and Feinberg, A. W., “Development of Polydimethylsiloxane Substrates with Tunable Elastic Modulus to Study Cell Mechanobiology in Muscle and Nerve,” PLoS One, Vol. 7, No. 12, Paper No. e51499, 2012.

    Article  Google Scholar 

  38. Dembo, M. and Wang, Y.-L., “Stresses at the Cell-to-Substrate Interface during Locomotion of Fibroblasts,” Biophysical Journal, Vol. 76, No. 4, pp. 2307–2316, 1999.

    Article  Google Scholar 

  39. Style, R. W., Boltyanskiy, R., German, G. K., Hyland, C., MacMinn, C.W., et al., “Traction Force Microscopy in Physics and Biology,” Soft Matter, Vol. 10, No. 23, pp. 4047–4055, 2014.

    Article  Google Scholar 

  40. Schwarz, U. S., Balaban, N. Q., Riveline, D., Bershadsky, A., Geiger, B., and Safran, S., “Calculation of Forces at Focal Adhesions from Elastic Substrate Data: The Effect of Localized Force and the Need for Regularization,” Biophysical Journal, Vol. 83, No. 3, pp. 1380–1394, 2002.

    Article  Google Scholar 

  41. Doyle, A. D. and Lee, J., “Simultaneous, Real-Time Imaging of Intracellular Calcium and Cellular Traction Force Production,” Biotechniques, Vol. 33, No. 2, pp. 358–365, 2002.

    Google Scholar 

  42. Roy, P., Petroll, W. M., Cavanagh, H. D., Chuong, C. J., and Jester, J. V., “An in Vitro Force Measurement Assay to Study the Early Mechanical Interaction between Corneal Fibroblasts and Collagen Matrix,” Experimental Cell Research, Vol. 232, No. 1, pp. 106–117, 1997.

    Article  Google Scholar 

  43. Koch, T. M., Münster, S., Bonakdar, N., Butler, J. P., and Fabry, B., “3D Traction Forces in Cancer Cell Invasion,” PLoS One, Vol. 7, No. 3, Paper No. e33476, 2012.

    Article  Google Scholar 

  44. Da Cunha, C. B., Klumpers, D. D., Li, W. A., Koshy, S. T., Weaver, J. C., et al., “Influence of the Stiffness of Three-Dimensional Alginate/Collagen-I Interpenetrating Networks on Fibroblast Biology,” Biomaterials, Vol. 35, No. 32, pp. 8927–8936, 2014.

    Article  Google Scholar 

  45. Shu, X. Z., Liu, Y., Palumbo, F. S., Luo, Y., and Prestwich, G. D., “In Situ Crosslinkable Hyaluronan Hydrogels for Tissue Engineering,” Biomaterials, Vol. 25, No. 7, pp. 1339–1348, 2004.

    Google Scholar 

  46. Baier Leach, J., Bivens, K. A., Patrick, C. W., and Schmidt, C. E., “Photocrosslinked Hyaluronic Acid Hydrogels: Natural, Biodegradable Tissue Engineering Scaffolds,” Biotechnology and Bioengineering, Vol. 82, No. 5, pp. 578–589, 2003.

    Article  Google Scholar 

  47. Park, Y. D., Tirelli, N., and Hubbell, J. A., “Photopolymerized Hyaluronic Acid-based Hydrogels and Interpenetrating Networks,” Biomaterials, Vol. 24, No. 6, pp. 893–900, 2003.

    Article  Google Scholar 

  48. Gerecht, S., Burdick, J. A., Ferreira, L. S., Townsend, S. A., Langer, R., and Vunjak-Novakovic, G., “Hyaluronic Acid Hydrogel for Controlled Self-Renewal and Differentiation of Human Embryonic Stem Cells,” Proceedings of the National Academy of Sciences, Vol. 104, No. 27, pp. 11298–11303, 2007.

    Article  Google Scholar 

  49. Chung, C. and Burdick, J. A., “Influence of Three-Dimensional Hyaluronic Acid Microenvironments on Mesenchymal Stem Cell Chondrogenesis,” Tissue Engineering Part A, Vol. 15, No. 2, pp. 243–254, 2008.

    Article  Google Scholar 

  50. Burdick, J. A., Chung, C., Jia, X., Randolph, M. A., and Langer, R., “Controlled Degradation and Mechanical Behavior of Photopolymerized Hyaluronic Acid Networks,” Biomacromolecules, Vol. 6, No. 1, pp. 386–391, 2005.

    Article  Google Scholar 

  51. Schanté, C. E., Zuber, G., Herlin, C., and Vandamme, T. F., “Chemical Modifications of Hyaluronic Acid for the Synthesis of Derivatives for a Broad Range of Biomedical Applications,” Carbohydrate Polymers, Vol. 85, No. 3, pp. 469–489, 2011.

    Article  Google Scholar 

  52. Hahn, M. S., McHale, M. K., Wang, E., Schmedlen, R. H., and West, J. L., “Physiologic Pulsatile Flow Bioreactor Conditioning of Poly (Ethylene Glycol)-based Tissue Engineered Vascular Grafts,” Annals of Biomedical Engineering, Vol. 35, No. 2, pp. 190–200, 2007.

    Article  Google Scholar 

  53. Hahn, M. S., Miller, J. S., and West, J. L., “Laser Scanning Lithography for Surface Micropatterning on Hydrogels,” Advanced Materials, Vol. 17, No. 24, pp. 2939–2942, 2005.

    Article  Google Scholar 

  54. Choi, J. H., Jin, H. K., Bae, J.-S., Park, C. W., Cheong, I. W., and Kim, G. M., Fabrication of Detachable Hydrogel Microplates for Separably Patterned Cell Culture, Int. J. Precis. Eng. Manuf., Vol. 15, No. 5, pp. 945–948, 2014.

  55. Gobin, A. S. and West, J. L., “Cell Migration through Defined, Synthetic ECM Analogs,” The FASEB Journal, Vol. 16, No. 7, pp. 751–753, 2002.

    Google Scholar 

  56. Fu, J., Wang, Y.-K., Yang, M. T., Desai, R. A., Yu, X., et al., “Mechanical Regulation of Cell Function with Geometrically Modulated Elastomeric Substrates,” Nature Methods, Vol. 7, No. 9, pp. 733–736, 2010.

    Article  Google Scholar 

  57. Lo, C.-M., Wang, H.-B., Dembo, M., and Wang, Y.-l., “Cell Movement is Guided by the Rigidity of the Substrate,” Biophysical Journal, Vol. 79, No. 1, pp. 144–152, 2000.

    Article  Google Scholar 

  58. Maeda, E., Sugimoto, M., and Ohashi, T., “Cytoskeletal Tension Modulates MMP-1 Gene Expression from Tenocytes on Micropillar Substrates,” Journal of Biomechanics, Vol. 46, No. 5, pp. 991–997, 2013.

    Article  Google Scholar 

  59. Trichet, L., Le Digabel, J., Hawkins, R. J., Vedula, S. R. K., Gupta, M., et al., “Evidence of a Large-Scale Mechanosensing Mechanism for Cellular Adaptation to Substrate Stiffness,” Proceedings of the National Academy of Sciences, Vol. 109, No. 18, pp. 6933–6938, 2012.

    Article  Google Scholar 

  60. Cui, Y., Hameed, F. M., Yang, B., Lee, K., Pan, C. Q., et al., “Cyclic Stretching of Soft Substrates Induces Spreading and Growth,” Nature Communications, Vol. 6, Paper No. 6333, 2015.

    Article  Google Scholar 

  61. Wang, J. H.-C. and Thampatty, B. P., “An Introductory Review of Cell Mechanobiology,” Biomechanics and Modeling in Mechanobiology, Vol. 5, No. 1, pp. 1–16, 2006.

    Article  Google Scholar 

  62. Krishnan, R., Park, C. Y., Lin, Y.-C., Mead, J., Jaspers, R. T., et al., “Reinforcement Versus Fluidization in Cytoskeletal Mechanoresponsiveness,” PLoS One, Vol. 4, No. 5, Paper No. e5486, 2009.

    Article  Google Scholar 

  63. Riehl, B. D., Park, J.-H., Kwon, I. K., and Lim, J. Y., “Mechanical Stretching for Tissue Engineering: Two-Dimensional and Three-Dimensional Constructs,” Tissue Engineering Part B: Reviews, Vol. 18, No. 4, pp. 288–300, 2012.

    Article  Google Scholar 

  64. Lee, H.-Y., Bae, J.-H., and Chang, S.-H., “Mechano-Regulation Theory-based Finite Element Analysis on the Effects of Driving Strain History on Cellular Differentiation, Int. J. Precis. Eng. Manuf., Vol. 16, No. 8, pp. 1851–1858, 2015.

    Article  Google Scholar 

  65. Casares, L., Vincent, R., Zalvidea, D., Campillo, N., Navajas, D., et al., “Hydraulic Fracture during Epithelial Stretching,” Nature Materials, Vol. 14, No. 3, pp. 343–351, 2015.

    Article  Google Scholar 

  66. Gavara, N., Roca-Cusachs, P., Sunyer, R., Farré, R., and Navajas, D., “Mapping Cell-Matrix Stresses during Stretch Reveals Inelastic Reorganization of the Cytoskeleton,” Biophysical Journal, Vol. 95, No. 1, pp. 464–471, 2008.

    Article  Google Scholar 

  67. Mann, J. M., Lam, R. H., Weng, S., Sun, Y., and Fu, J., “A Siliconebased Stretchable Micropost Array Membrane for Monitoring Live-Cell Subcellular Cytoskeletal Response,” Lab on a Chip, Vol. 12, No. 4, pp. 731–740, 2012.

    Article  Google Scholar 

  68. Tang, J., Li, J., Vlassak, J. J., and Suo, Z., “Adhesion between Highly Stretchable Materials,” Soft Matter, Vol. 12, No. 4, pp. 1093–1099, 2016.

    Article  Google Scholar 

  69. Trepat, X., Deng, L., An, S. S., Navajas, D., Tschumperlin, D. J., et al., “Universal Physical Responses to Stretch in the Living Cell,” Nature, Vol. 447, No. 7144, pp. 592–595, 2007.

    Article  Google Scholar 

  70. Park, J.-A., Fredberg, J. J., and Drazen, J. M., “Putting the Squeeze on Airway Epithelia,” Physiology, Vol. 30, No. 4, pp. 293–303, 2015.

    Article  Google Scholar 

  71. Tschumperlin, D. J., Dai, G., Maly, I. V., Kikuchi, T., Laiho, L. H., et al., “Mechanotransduction through Growth-Factor Shedding into the Extracellular Space,” Nature, Vol. 429, No. 6987, pp. 83–86, 2004.

    Article  Google Scholar 

  72. Ressler, B., Lee, R. T., Randell, S. H., Drazen, J. M., and Kamm, R. D., “Molecular Responses of Rat Tracheal Epithelial Cells to Transmembrane Pressure,” American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 278, No. 6, pp. L1264–L1272, 2000.

    Google Scholar 

  73. Tschumperlin, D. J., Shively, J. D., Swartz, M. A., Silverman, E. S., Haley, K. J., et al., “Bronchial Epithelial Compression Regulates MAP Kinase Signaling and HB-EGF-like Growth Factor Expression,” American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 282, No. 5, pp. L904–L911, 2002.

    Article  Google Scholar 

  74. Sadati, M., Nourhani, A., Fredberg, J. J., and Taheri Qazvini, N., “Glass-like Dynamics in the Cell and in Cellular Collectives,” Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 6, No. 2, pp. 137–149, 2014.

    Google Scholar 

  75. Sadati, M., Qazvini, N. T., Krishnan, R., Park, C. Y., and Fredberg, J. J., “Collective Migration and Cell Jamming,” Differentiation, Vol. 86, No. 3, pp. 121–125, 2013.

    Article  Google Scholar 

  76. Park, J.-A., Kim, J. H., Bi, D., Mitchel, J. A., Qazvini, N. T., et al., “Unjamming and Cell Shape in the Asthmatic Airway Epithelium,” Nature Materials, Vol. 14, No. 10, pp. 1040–1048, 2015.

    Article  Google Scholar 

  77. Wu, J., Mao, Z., Tan, H., Han, L., Ren, T., and Gao, C., “Gradient Biomaterials and their Influences on Cell Migration,” Interface Focus, Vol. 2, No. 3, pp. 337–355, 2012.

    Article  Google Scholar 

  78. Rot, A. and von Andrian, U. H., “Chemokines in Innate and Adaptive Host Defense: Basic Chemokinese Grammar for Immune Cells,” Annual Review of Immunology, Vol. 22, pp. 891–928, 2004.

    Article  Google Scholar 

  79. Devreotes, P. and Janetopoulos, C., “Eukaryotic Chemotaxis: Distinctions between Directional Sensing and Polarization,” Journal of Biological Chemistry, Vol. 278, No. 23, pp. 20445–20448, 2003.

    Article  Google Scholar 

  80. Kim, M., Gweon, B., Koh, U., Cho, Y., Shin, D. W., et al., Matrix Stiffness Induces Epithelial Mesenchymal Transition Phenotypes of Human Epidermal Keratinocytes on Collagen Coated Two Dimensional Cell Culture, Biomedical Engineering Letters, Vol. 5, No. 3, pp. 194–202, 2015.

  81. Rodriguez, L. L. and Schneider, I. C., “Directed Cell Migration in Multi-Cue Environments,” Integrative Biology, Vol. 5, No. 11, pp. 1306–1323, 2013.

    Article  Google Scholar 

  82. Swartz, M. A. and Fleury, M. E., “Interstitial Flow and Its Effects in Soft Tissues,” Annual Review of Biomedical Engineering, Vol. 9, pp. 229–256, 2007.

    Article  Google Scholar 

  83. Li, J. and Lin, F., “Microfluidic Devices for Studying Chemotaxis and Electrotaxis,” Trends in Cell Biology, Vol. 21, No. 8, pp. 489–497, 2011.

    Article  Google Scholar 

  84. Somaweera, H., Ibraguimov, A., and Pappas, D., “A Review of Chemical Gradient Systems for Cell Analysis,” Analytica chimica acta, Vol. 907, pp. 7–17, 2016.

    Article  Google Scholar 

  85. Bastounis, E., Meili, R., Álvarez-González, B., Francois, J., del Álamo, J. C., et al., “Both Contractile Axial and Lateral Traction Force Dynamics Drive Amoeboid Cell Motility,” The Journal of Cell Biology, Vol. 204, No. 6, pp. 1045–1061, 2014.

    Article  Google Scholar 

  86. Smith, L. A., Aranda-Espinoza, H., Haun, J. B., Dembo, M., and Hammer, D. A., “Neutrophil Traction Stresses are Concentrated in the Uropod during Migration,” Biophysical Journal, Vol. 92, No. 7, pp. L58–L60, 2007.

    Article  Google Scholar 

  87. Jannat, R. A., Dembo, M., and Hammer, D. A., “Traction Forces of Neutrophils Migrating on Compliant Substrates,” Biophysical Journal, Vol. 101, No. 3, pp. 575–584, 2011.

    Article  Google Scholar 

  88. Jannat, R. A., Robbins, G. P., Ricart, B. G., Dembo, M., and Hammer, D. A., “Neutrophil Adhesion and Chemotaxis Depend on Substrate Mechanics,” Journal of Physics: Condensed Matter, Vol. 22, No. 19, Paper No. 194117, 2010.

    Google Scholar 

  89. Ricart, B. G., Yang, M. T., Hunter, C. A., Chen, C. S., and Hammer, D. A., “Measuring Traction Forces of Motile Dendritic Cells on Micropost Arrays,” Biophysical Journal, Vol. 101, No. 11, pp. 2620–2628, 2011.

    Article  Google Scholar 

  90. Wen, J. H., Choi, O., Taylor-Weiner, H., Fuhrmann, A., Karpiak, J. V., et al., “Haptotaxis is Cell Type Specific and Limited by Substrate Adhesiveness,” Cellular and Molecular Bioengineering, Vol. 8, No. 4, pp. 530–542, 2015.

    Article  Google Scholar 

  91. Gaudet, C., Marganski, W. A., Kim, S., Brown, C. T., Gunderia, V., et al., “Influence of Type I Collagen Surface Density on Fibroblast Spreading, Motility, and Contractility,” Biophysical Journal, Vol. 85, No. 5, pp. 3329–3335, 2003.

    Article  Google Scholar 

  92. Rajagopalan, P., Marganski, W. A., Brown, X. Q., and Wong, J. Y., “Direct Comparison of the Spread Area, Contractility, and Migration of Balb/C 3T3 Fibroblasts Adhered to Fibronectin-and RGD-Modified Substrata,” Biophysical journal, Vol. 87, No. 4, pp. 2818–2827, 2004.

    Article  Google Scholar 

  93. McCaig, C. D., Rajnicek, A. M., Song, B., and Zhao, M., “Controlling Cell Behavior Electrically: Current Views and Future Potential,” Physiological Reviews, Vol. 85, No. 3, pp. 943–978, 2005.

    Article  Google Scholar 

  94. Nakajima, K.-I., Zhu, K., Sun, Y.-H., Hegyi, B., Zeng, Q., et al., “KCNJ15/KIR4.2 Couples with Polyamines to Sense Weak Extracellular Electric Fields in Galvanotaxis,” Nature Communications, Vol. 6, Article No. 8532, DOI No. 10.1038/ncomms9532, 2015.

    Article  Google Scholar 

  95. Zhao, M., “Electrical Fields In Wound Healing-An Overriding Signal that Directs Cell Migration,” Seminars in Cell & Developmental Biology, Vol. 20, No. 6, pp. 674–682, 2009.

    Article  Google Scholar 

  96. Haeger, A., Wolf, K., Zegers, M. M., and Friedl, P., “Collective Cell Migration: Guidance Principles and Hierarchies,” Trends in Cell Biology, Vol. 25, No. 9, pp. 556–566, 2015.

    Article  Google Scholar 

  97. Trepat, X., Wasserman, M. R., Angelini, T. E., Millet, E., Weitz, D. A., et al., “Physical Forces during Collective Cell Migration,” Nature Physics, Vol. 5, No. 6, pp. 426–430, 2009.

    Article  Google Scholar 

  98. Kim, J. H., Serra-Picamal, X., Tambe, D. T., Zhou, E. H., Park, C. Y., et al., “Propulsion and Navigation within the Advancing Monolayer Sheet,” Nature Materials, Vol. 12, No. 9, pp. 856–863, 2013.

    Article  Google Scholar 

  99. Tambe, D. T., Hardin, C. C., Angelini, T. E., Rajendran, K., Park, C. Y., et al., “Collective Cell Guidance by Cooperative Intercellular Forces,” Nature Materials, Vol. 10, No. 6, pp. 469–475, 2011.

    Article  Google Scholar 

  100. Cortese, B., Palamà, I. E., D’Amone, S., and Gigli, G., “Influence of Electrotaxis on Cell Behaviour,” Integrative Biology, Vol. 6, No. 9, pp. 817–830, 2014.

    Article  Google Scholar 

  101. Cohen, D. J., Nelson, W. J., and Maharbiz, M. M., “Galvanotactic Control of Collective Cell Migration in Epithelial Monolayers,” Nature Materials, Vol. 13, No. 4, pp. 409–417, 2014.

    Article  Google Scholar 

  102. Song, B., Gu, Y., Pu, J., Reid, B., Zhao, Z., and Zhao, M., “Application of Direct Current Electric Fields to Cells and Tissues in vitro and Modulation of Wound Electric Field in Vivo,” Nature Protocols, Vol. 2, No. 6, pp. 1479–1489, 2007.

    Article  Google Scholar 

  103. Li, L., Hartley, R., Reiss, B., Sun, Y., Pu, J., et al., “E-Cadherin Plays an Essential Role in Collective Directional Migration of Large Epithelial Sheets,” Cellular and Molecular Life Sciences, Vol. 69, No. 16, pp. 2779–2789, 2012.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Mechanical Engineering, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon, 34141, South Korea

    Youngbin Cho, Eun Young Park, Eunmin Ko, Jin-Sung Park & Jennifer H. Shin

Authors
  1. Youngbin Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eun Young Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eunmin Ko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jin-Sung Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jennifer H. Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer H. Shin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cho, Y., Park, E.Y., Ko, E. et al. Recent advances in biological uses of traction force microscopy. Int. J. Precis. Eng. Manuf. 17, 1401–1412 (2016). https://doi.org/10.1007/s12541-016-0166-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12541-016-0166-x

Keywords

Search

Navigation