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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
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
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Jo, H. and Shin, J. H., “Special Issue on Mechanobiology and Diseases, Biomedical Engineering Letters, Vol. 5, No. 3, pp. 159–161, 2015.
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.
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.
Davies, P. F., “Flow-Mediated Endothelial Mechanotransduction,” Physiological Reviews, Vol. 75, No. 3, pp. 519–560, 1995.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Rodriguez, L. L. and Schneider, I. C., “Directed Cell Migration in Multi-Cue Environments,” Integrative Biology, Vol. 5, No. 11, pp. 1306–1323, 2013.
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.
Li, J. and Lin, F., “Microfluidic Devices for Studying Chemotaxis and Electrotaxis,” Trends in Cell Biology, Vol. 21, No. 8, pp. 489–497, 2011.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12541-016-0166-x