Technical Forum

Measurement Systems for Cell Adhesive Forces

[+] Author and Article Information
Dennis W. Zhou

Wallace H. Coulter Department
of Biomedical Engineering,
Petit Institute for Bioengineering
and Bioscience,
Georgia Institute of Technology,
Atlanta, GA 30332
e-mail: dzhou@gatech.edu

Andrés J. García

Woodruff School of Mechanical Engineering,
Petit Institute for Bioengineering and Bioscience,
Georgia Institute of Technology,
Atlanta, GA 30332
e-mail: andres.garcia@me.gatech.edu

1Corresponding author.

Manuscript received August 12, 2014; final manuscript received November 18, 2014; published online January 26, 2015. Editor: Beth Winkelstein.

J Biomech Eng 137(2), 020908 (Feb 01, 2015) (8 pages) Paper No: BIO-14-1387; doi: 10.1115/1.4029210 History: Received August 12, 2014; Revised November 18, 2014; Online January 26, 2015

Cell adhesion to the extracellular matrix (ECM) involves integrin receptor–ligand binding and clustering to form focal adhesion (FA) complexes, which mechanically link the cell’s cytoskeleton to the ECM and regulate fundamental cell signaling pathways. Although elucidation of the biochemical events in cell-matrix adhesive interactions is rapidly advancing, recent studies show that the forces underlying cell-matrix adhesive interactions are also critical to cell responses. Therefore, multiple measurement systems have been developed to quantify the spatial and temporal dynamics of cell adhesive forces, and these systems have identified how mechanical events influence cell phenotype and FA structure–function relationships under physiological and pathological settings. This review focuses on the development, methodology, and applications of measurement systems for probing (a) cell adhesion strength and (b) 2D and 3D cell traction forces.

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Humphries, J. D., Byron, A., and Humphries, M. J., 2006, “Integrin Ligands at a Glance,” J. Cell Sci., 119(Pt. 19), pp. 3901–3903. [CrossRef] [PubMed]
Humphries, J. D., Byron, A., Bass, M. D., Craig, S. E., Pinney, J. W., Knight, D., and Humphries, M. J., 2009, “Proteomic Analysis of Integrin-Associated Complexes Identifies RCC2 as a Dual Regulator of Rac1 and Arf6,” Sci. Signal., 2(87), p. ra51. [CrossRef] [PubMed]
Dumbauld, D. W., Lee, T. T., Singh, A., Scrimgeour, J., Gersbach, C. A., Zamir, E. A., Fu, J., Chen, C. S., Curtis, J. E., Craig, S. W., and Garcia, A. J., 2013, “How Vinculin Regulates Force Transmission,” Proc. Natl. Acad. Sci. U. S. A., 110(24), pp. 9788–9793. [CrossRef] [PubMed]
Xu, W., Baribault, H., and Adamson, E. D., 1998, “Vinculin Knockout Results in Heart and Brain Defects During Embryonic Development,” Development, 125(2), pp. 327–337. [PubMed]
Shen, M., and Horbett, T. A., 2001, “The Effects of Surface Chemistry and Adsorbed Proteins on Monocyte/Macrophage Adhesion to Chemically Modified Polystyrene Surfaces,” J. Biomed. Mater. Res., 57(3), pp. 336–345. [CrossRef] [PubMed]
Huynh, J., Nishimura, N., Rana, K., Peloquin, J. M., Califano, J. P., Montague, C. R., King, M. R., Schaffer, C. B., and Reinhart-King, C. A., 2011, “Age-Related Intimal Stiffening Enhances Endothelial Permeability and Leukocyte Transmigration,” Sci. Transl. Med., 3(112), p. 112ra122. [CrossRef] [PubMed]
Mcever, R. P., 2001, “Adhesive Interactions of Leukocytes, Platelets, and the Vessel Wall During Hemostasis and Inflammation,” Thromb. Haemostasis, 86(3), pp. 746–756.
Kraning-Rush, C. M., Califano, J. P., and Reinhart-King, C. A., 2012, “Cellular Traction Stresses Increase With Increasing Metastatic Potential,” PLoS One, 7(2), p. e32572. [CrossRef] [PubMed]
Yang, M. T., Fu, J., Wang, Y. K., Desai, R. A., and Chen, C. S., 2011, “Assaying Stem Cell Mechanobiology on Microfabricated Elastomeric Substrates With Geometrically Modulated Rigidity,” Nat. Protoc., 6(2), pp. 187–213. [CrossRef] [PubMed]
Cohen, D. M., Yang, M. T., and Chen, C. S., 2013, “Measuring Cell-Cell Tugging Forces Using Bowtie-Patterned Mpads (Microarray Post Detectors),” Methods Mol. Biol., 1066, pp. 157–168. [CrossRef] [PubMed]
Heisenberg, C. P., and Bellaiche, Y., 2013, “Forces in Tissue Morphogenesis and Patterning,” Cell, 153(5), pp. 948–962. [CrossRef] [PubMed]
Gallant, N. D., and Garcia, A. J., 2007, “Quantitative Analyses of Cell Adhesion Strength,” Methods Mol. Biol., 370, pp. 83–96. [CrossRef] [PubMed]
Garcia, A. J., and Gallant, N. D., 2003, “Stick and Grip: Measurement Systems and Quantitative Analyses of Integrin-Mediated Cell Adhesion Strength,” Cell Biochem. Biophys., 39(1), pp. 61–73. [CrossRef] [PubMed]
Coyer, S. R., Singh, A., Dumbauld, D. W., Calderwood, D. A., Craig, S. W., Delamarche, E., and Garcia, A. J., 2012, “Nanopatterning Reveals an ECM Area Threshold for Focal Adhesion Assembly and Force Transmission That Is Regulated by Integrin Activation and Cytoskeleton Tension,” J. Cell Sci., 125(Pt. 21), pp. 5110–5123. [CrossRef] [PubMed]
Gallant, N. D., Michael, K. E., and Garcia, A. J., 2005, “Cell Adhesion Strengthening: Contributions of Adhesive Area, Integrin Binding, and Focal Adhesion Assembly,” Mol. Biol. Cell, 16(9), pp. 4329–4340. [CrossRef] [PubMed]
Amano, M., Chihara, K., Kimura, K., Fukata, Y., Nakamura, N., Matsuura, Y., and Kaibuchi, K., 1997, “Formation of Actin Stress Fibers and Focal Adhesions Enhanced by Rho-Kinase,” Science, 275(5304), pp. 1308–1311. [CrossRef] [PubMed]
Marshall, B. T., Long, M., Piper, J. W., Yago, T., Mcever, R. P., and Zhu, C., 2003, “Direct Observation of Catch Bonds Involving Cell-Adhesion Molecules,” Nature, 423(6936), pp. 190–193. [CrossRef] [PubMed]
Evans, E., Leung, A., Heinrich, V., and Zhu, C., 2004, “Mechanical Switching and Coupling Between Two Dissociation Pathways in a P-Selectin Adhesion Bond,” Proc. Natl. Acad. Sci. U. S. A., 101(31), pp. 11281–11286. [CrossRef] [PubMed]
Mcclay, D. R., Wessel, G. M., and Marchase, R. B., 1981, “Intercellular Recognition: Quantitation of Initial Binding Events,” Proc. Natl. Acad. Sci. U. S. A., 78(8), pp. 4975–4979. [CrossRef] [PubMed]
Prechtel, K., Bausch, A. R., Marchi-Artzner, V., Kantlehner, M., Kessler, H., and Merkel, R., 2002, “Dynamic Force Spectroscopy to Probe Adhesion Strength of Living Cells,” Phys. Rev. Lett., 89(2), p. 028101. [CrossRef] [PubMed]
Tozeren, A., Sung, K. L., and Chien, S., 1989, “Theoretical and Experimental Studies on Cross-Bridge Migration During Cell Disaggregation,” Biophys. J., 55(3), pp. 479–487. [CrossRef] [PubMed]
Litvinov, R. I., Shuman, H., Bennett, J. S., and Weisel, J. W., 2002, “Binding Strength and Activation State of Single Fibrinogen-Integrin Pairs on Living Cells,” Proc. Natl. Acad. Sci. U. S. A., 99(11), pp. 7426–7431. [CrossRef] [PubMed]
Roca-Cusachs, P., Gauthier, N. C., Del Rio, A., and Sheetz, M. P., 2009, “Clustering of Alpha(5)Beta(1) Integrins Determines Adhesion Strength Whereas Alpha(V)Beta(3) and Talin Enable Mechanotransduction,” Proc. Natl. Acad. Sci. U. S. A., 106(38), pp. 16245–16250. [CrossRef] [PubMed]
Jiang, G., Giannone, G., Critchley, D. R., Fukumoto, E., and Sheetz, M. P., 2003, “Two-Piconewton Slip Bond Between Fibronectin and the Cytoskeleton Depends on Talin,” Nature, 424(6946), pp. 334–337. [CrossRef] [PubMed]
Kong, F., Li, Z., Parks, W. M., Dumbauld, D. W., Garcia, A. J., Mould, A. P., Humphries, M. J., and Zhu, C., 2013, “Cyclic Mechanical Reinforcement of Integrin-Ligand Interactions,” Mol. Cell, 49(6), pp. 1060–1068. [CrossRef] [PubMed]
Kong, F., Garcia, A. J., Mould, A. P., Humphries, M. J., and Zhu, C., 2009, “Demonstration of Catch Bonds Between an Integrin and Its Ligand,” J. Cell Biol., 185(7), pp. 1275–1284. [CrossRef] [PubMed]
Reyes, C. D., and Garcia, A. J., 2003, “A Centrifugation Cell Adhesion Assay for High-Throughput Screening of Biomaterial Surfaces,” J. Biomed. Mater. Res., Part A, 67(1), pp. 328–333. [CrossRef]
Keselowsky, B. G., Collard, D. M., and Garcia, A. J., 2003, “Surface Chemistry Modulates Fibronectin Conformation and Directs Integrin Binding and Specificity to Control Cell Adhesion,” J. Biomed. Mater. Res., Part A,66(2), pp. 247–259. [CrossRef]
Doroszewski, J., Skierski, J., and Przadka, L., 1977, “Interaction of Neoplastic Cells With Glass Surface Under Flow Conditions,” Exp. Cell Res., 104(2), pp. 335–343. [CrossRef] [PubMed]
Truskey, G. A., and Pirone, J. S., 1990, “The Effect of Fluid Shear Stress Upon Cell Adhesion to Fibronectin-Treated Surfaces,” J. Biomed. Mater. Res., 24(10), pp. 1333–1353. [CrossRef] [PubMed]
Van Kooten, T. G., Schakenraad, J. M., Van Der Mei, H. C., and Busscher, H. J., 1992, “Development and Use of a Parallel-Plate Flow Chamber for Studying Cellular Adhesion to Solid Surfaces,” J. Biomed. Mater. Res., 26(6), pp. 725–738. [CrossRef] [PubMed]
Lawrence, M. B., Mcintire, L. V., and Eskin, S. G., 1987, “Effect of Flow on Polymorphonuclear Leukocyte/Endothelial Cell Adhesion,” Blood, 70(5), pp. 1284–1290. [PubMed]
Cozens-Roberts, C., Quinn, J. A., and Lauffenberger, D. A., 1990, “Receptor-Mediated Adhesion Phenomena. Model Studies With the Radical-Flow Detachment Assay,” Biophys. J., 58(1), pp. 107–125. [CrossRef] [PubMed]
Mohandas, N., Hochmuth, R. M., and Spaeth, E. E., 1974, “Adhesion of Red Cells to Foreign Surfaces in the Presence of Flow,” J. Biomed. Mater. Res., 8(2), pp. 119–136. [CrossRef] [PubMed]
Garcia, A. J., Huber, F., and Boettiger, D., 1998, “Force Required to Break Alpha5beta1 Integrin-Fibronectin Bonds in Intact Adherent Cells Is Sensitive to Integrin Activation State,” J. Biol. Chem., 273(18), pp. 10988–10993. [CrossRef] [PubMed]
Usami, S., Chen, H. H., Zhao, Y., Chien, S., and Skalak, R., 1993, “Design and Construction of a Linear Shear Stress Flow Chamber,” Ann. Biomed. Eng., 21(1), pp. 77–83. [CrossRef] [PubMed]
Bundy, K. J., Harris, L. G., Rahn, B. A., and Richards, R. G., 2001, “Measurement of Fibroblast and Bacterial Detachment From Biomaterials Using Jet Impingement,” Cell Biol. Int., 25(4), pp. 289–307. [CrossRef] [PubMed]
Burmeister, J. S., Vrany, J. D., Reichert, W. M., and Truskey, G. A., 1996, “Effect of Fibronectin Amount and Conformation on the Strength of Endothelial Cell Adhesion to Hema/Ema Copolymers,” J. Biomed. Mater. Res., 30(1), pp. 13–22. [CrossRef] [PubMed]
Garcia, A. J., Ducheyne, P., and Boettiger, D., 1997, “Quantification of Cell Adhesion Using a Spinning Disc Device and Application to Surface-Reactive Materials,” Biomaterials, 18(16), pp. 1091–1098. [CrossRef] [PubMed]
Michael, K. E., and García, A. J., 2007, “Cell Adhesion Strengthening: Measurement and Analysis,” Methods Cell Biol., 83, pp. 329–346. [CrossRef] [PubMed]
Friedland, J. C., Lee, M. H., and Boettiger, D., 2009, “Mechanically Activated Integrin Switch Controls Alpha5beta1 Function,” Science, 323(5914), pp. 642–644. [CrossRef] [PubMed]
Engler, A. J., Chan, M., Boettiger, D., and Schwarzbauer, J. E., 2009, “A Novel Mode of Cell Detachment From Fibrillar Fibronectin Matrix Under Shear,” J. Cell Sci., 122(Pt. 10), pp. 1647–1653. [CrossRef] [PubMed]
Singh, A., Suri, S., Lee, T., Chilton, J. M., Cooke, M. T., Chen, W. Q., Fu, J. P., Stice, S. L., Lu, H., Mcdevitt, T. C., and Garcia, A. J., 2013, “Adhesion Strength-Based, Label-Free Isolation of Human Pluripotent Stem Cells,” Nat. Methods, 10(5), pp. 438–444. [CrossRef] [PubMed]
Dembo, M., and Wang, Y. L., 1999, “Stresses at the Cell-to-Substrate Interface During Locomotion of Fibroblasts,” Biophys. J., 76(4), pp. 2307–2316. [CrossRef] [PubMed]
Harris, A. K., Wild, P., and Stopak, D., 1980, “Silicone Rubber Substrata: A New Wrinkle in the Study of Cell Locomotion,” Science, 208(4440), pp. 177–179. [CrossRef] [PubMed]
Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K., and Chen, C. S., 2003, “Cells Lying on a Bed of Microneedles: An Approach to Isolate Mechanical Force,” Proc. Natl. Acad. Sci. U. S. A., 100(4), pp. 1484–1489. [CrossRef] [PubMed]
Sabass, B., Gardel, M. L., Waterman, C. M., and Schwarz, U. S., 2008, “High Resolution Traction Force Microscopy Based on Experimental and Computational Advances,” Biophys. J., 94(1), pp. 207–220. [CrossRef] [PubMed]
Plotnikov, S. V., Sabass, B., Schwarz, U. S., and Waterman, C. M., 2014, “High-Resolution Traction Force Microscopy,” Methods Cell. Biol., 123, pp. 367–394. [CrossRef] [PubMed]
Califano, J. P., and Reinhart-King, C. A., 2010, “Substrate Stiffness and Cell Area Predict Cellular Traction Stresses in Single Cells and Cells in Contact,” Cell. Mol. Bioeng., 3(1), pp. 68–75. [CrossRef] [PubMed]
Reinhart-King, C. A., Dembo, M., and Hammer, D. A., 2003, “Endothelial Cell Traction Forces on Rgd-Derivatized Polyacrylamide Substrata,” Langmuir, 19(5), pp. 1573–1579. [CrossRef]
Reinhart-King, C. A., Dembo, M., and Hammer, D. A., 2005, “The Dynamics and Mechanics of Endothelial Cell Spreading,” Biophys. J., 89(1), pp. 676–689. [CrossRef] [PubMed]
Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E., 2006, “Matrix Elasticity Directs Stem Cell Lineage Specification,” Cell, 126(4), pp. 677–89. [CrossRef] [PubMed]
Isenberg, B. C., Dimilla, P. A., Walker, M., Kim, S., and Wong, J. Y., 2009, “Vascular Smooth Muscle Cell Durotaxis Depends on Substrate Stiffness Gradient Strength,” Biophys. J., 97(5), pp. 1313–1322. [CrossRef] [PubMed]
Gilbert, P. M., Havenstrite, K. L., Magnusson, K. E., Sacco, A., Leonardi, N. A., Kraft, P., Nguyen, N. K., Thrun, S., Lutolf, M. P., and Blau, H. M., 2010, “Substrate Elasticity Regulates Skeletal Muscle Stem Cell Self-Renewal in Culture,” Science, 329(5995), pp. 1078–1081. [CrossRef] [PubMed]
Huynh, J., Bordeleau, F., Kraning-Rush, C. M., and Reinhart-King, C. A., 2013, “Substrate Stiffness Regulates Pdgf-Induced Circular Dorsal Ruffle Formation Through MLCK,” Cell. Mol. Bioeng., 6(2), pp. 138–147. [CrossRef]
Califano, J. P., and Reinhart-King, C. A., 2009, “The Effects of Substrate Elasticity on Endothelial Cell Network Formation and Traction Force Generation,” 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vols. 1–20, pp. 3343–3345.
Chowdhury, F., Na, S., Li, D., Poh, Y. C., Tanaka, T. S., Wang, F., and Wang, N., 2010, “Material Properties of the Cell Dictate Stress-Induced Spreading and Differentiation in Embryonic Stem Cells,” Nat. Mater., 9(1), pp. 82–88. [CrossRef] [PubMed]
Wen, J. H., Vincent, L. G., Fuhrmann, A., Choi, Y. S., Hribar, K. C., Taylor-Weiner, H., Chen, S., and Engler, A. J., 2014, “Interplay of Matrix Stiffness and Protein Tethering in Stem Cell Differentiation,” Nat. Mater., 13(10), pp. 979–987. [CrossRef] [PubMed]
Gershlak, J. R., Resnikoff, J. I., Sullivan, K. E., Williams, C., Wang, R. M., and Black, and L. D., III, 2013, “Mesenchymal Stem Cells Ability to Generate Traction Stress in Response to Substrate Stiffness is Modulated by the Changing Extracellular Matrix Composition of the Heart During Development,” Biochem. Biophys. Res. Commun., 439(2), pp. 161–166. [CrossRef] [PubMed]
Li, B., Moshfegh, C., Lin, Z., Albuschies, J., and Vogel, V., 2013, “Mesenchymal Stem Cells Exploit Extracellular Matrix as Mechanotransducer,” Sci. Rep., 3, p. 2425. [CrossRef] [PubMed]
Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D., Hammer, D. A., and Weaver, V. M., 2005, “Tensional Homeostasis and the Malignant Phenotype,” Cancer Cell, 8(3), pp. 241–254. [CrossRef] [PubMed]
Yeung, T., Georges, P. C., Flanagan, L. A., Marg, B., Ortiz, M., Funaki, M., Zahir, N., Ming, W., Weaver, V., and Janmey, P. A., 2005, “Effects of Substrate Stiffness on Cell Morphology, Cytoskeletal Structure, and Adhesion,” Cell Motil. Cytoskeleton, 60(1), pp. 24–34. [CrossRef] [PubMed]
Ng, M. R., Besser, A., Danuser, G., and Brugge, J. S., 2012, “Substrate Stiffness Regulates Cadherin-Dependent Collective Migration Through Myosin-II Contractility,” J. Cell Biol., 199(3), pp. 545–563. [CrossRef] [PubMed]
Parsons, J. T., Horwitz, A. R., and Schwartz, M. A., 2010, “Cell Adhesion: Integrating Cytoskeletal Dynamics and Cellular Tension,” Nat. Rev. Mol. Cell Biol., 11(9), pp. 633–643. [CrossRef] [PubMed]
Pelham, R. J., Jr., and Wang, Y., 1997, “Cell Locomotion and Focal Adhesions Are Regulated by Substrate Flexibility,” Proc. Natl. Acad. Sci. U. S. A., 94(25), pp. 13661–13665. [CrossRef] [PubMed]
Galbraith, C. G., and Sheetz, M. P., 1997, “A Micromachined Device Provides a New Bend on Fibroblast Traction Forces,” Proc. Natl. Acad. Sci. U. S. A., 94(17), pp. 9114–9118. [CrossRef] [PubMed]
Sniadecki, N. J., and Chen, C. S., 2007, “Microfabricated Silicone Elastomeric Post Arrays for Measuring Traction Forces of Adherent Cells,” Methods Cell Biol., 83, pp. 313–328. [CrossRef] [PubMed]
Fu, J., Wang, Y. K., Yang, M. T., Desai, R. A., Yu, X., Liu, Z., and Chen, C. S., 2010, “Mechanical Regulation of Cell Function With Geometrically Modulated Elastomeric Substrates,” Nat. Methods, 7(9), pp. 733–736. [CrossRef] [PubMed]
Ting, L. H., Jahn, J. R., Jung, J. I., Shuman, B. R., Feghhi, S., Han, S. J., Rodriguez, M. L., and Sniadecki, N. J., 2012, “Flow Mechanotransduction Regulates Traction Forces, Intercellular Forces, and Adherens Junctions,” Am. J. Physiol.: Heart Circ. Physiol., 302(11), pp. H2220–H2220. [CrossRef] [PubMed]
Han, S. J., Bielawski, K. S., Ting, L. H., Rodriguez, M. L., and Sniadecki, N. J., 2012, “Decoupling Substrate Stiffness, Spread Area, and Micropost Density: A Close Spatial Relationship Between Traction Forces and Focal Adhesions,” Biophys. J., 103(4), pp. 640–648. [CrossRef] [PubMed]
Sniadecki, N. J., Han, S. J., Ting, L. H., and Feghhi, S., 2014, “Micropatterning on Micropost Arrays,” Methods Cell Biol., 121, pp. 61–73. [CrossRef] [PubMed]
Trichet, L., Le Digabel, J., Hawkins, R. J., Vedula, S. R., Gupta, M., Ribrault, C., Hersen, P., Voituriez, R., and Ladoux, B., 2012, “Evidence of a Large-Scale Mechanosensing Mechanism for Cellular Adaptation to Substrate Stiffness,” Proc. Natl. Acad. Sci. U. S. A., 109(18), pp. 6933–6938. [CrossRef] [PubMed]
Rabodzey, A., Alcaide, P., Luscinskas, F. W., and Ladoux, B., 2008, “Mechanical Forces Induced by the Transendothelial Migration of Human Neutrophils,” Biophys. J., 95(3), pp. 1428–1438. [CrossRef] [PubMed]
Saez, A., Anon, E., Ghibaudo, M., Du Roure, O., Di Meglio, J. M., Hersen, P., Silberzan, P., Buguin, A., and Ladoux, B., 2010, “Traction Forces Exerted by Epithelial Cell Sheets,” J. Phys.: Condens. Matter, 22(19), p. 194119. [CrossRef] [PubMed]
Brugues, A., Anon, E., Conte, V., Veldhuis, J. H., Gupta, M., Colombelli, J., Munoz, J. J., Brodland, G. W., Ladoux, B., and Trepat, X., 2014, “Forces Driving Epithelial Wound Healing,” Nat. Phys., 10(9), pp. 684–691. [CrossRef]
Liu, Y., Yehl, K., Narui, Y., and Salaita, K., 2013, “Tension Sensing Nanoparticles for Mechano-Imaging at the Living/Nonliving Interface,” J. Am. Chem. Soc., 135(14), pp. 5320–5323. [CrossRef] [PubMed]
Grashoff, C., Hoffman, B. D., Brenner, M. D., Zhou, R., Parsons, M., Yang, M. T., Mclean, M. A., Sligar, S. G., Chen, C. S., Ha, T., and Schwartz, M. A., 2010, “Measuring Mechanical Tension Across Vinculin Reveals Regulation of Focal Adhesion Dynamics,” Nature, 466(7303), pp. 263–236. [CrossRef] [PubMed]
Conway, D. E., Breckenridge, M. T., Hinde, E., Gratton, E., Chen, C. S., and Schwartz, M. A., 2013, “Fluid Shear Stress on Endothelial Cells Modulates Mechanical Tension Across Ve-Cadherin and Pecam-1,” Curr. Biol., 23(11), pp. 1024–1030. [CrossRef] [PubMed]
Woodfin, A., Voisin, M. B., and Nourshargh, S., 2007, “Pecam-1: A Multi-Functional Molecule in Inflammation and Vascular Biology,” Arterioscler, Thromb., Vasc. Biol., 27(12), pp. 2514–2523. [CrossRef]
Wang, X., and Ha, T., 2013, “Defining Single Molecular Forces Required to Activate Integrin and Notch Signaling,” Science, 340(6135), pp. 991–994. [CrossRef] [PubMed]
Baker, B. M., and Chen, C. S., 2012, “Deconstructing the Third Dimension: How 3D Culture Microenvironments Alter Cellular Cues,” J. Cell Sci., 125(Pt. 13), pp. 3015–3024. [CrossRef] [PubMed]
Schwartz, M. A., and Chen, C. S., 2013, “Cell Biology. Deconstructing Dimensionality,” Science, 339(6118), pp. 402–404. [CrossRef] [PubMed]
Fraley, S. I., Feng, Y., Krishnamurthy, R., Kim, D. H., Celedon, A., Longmore, G. D., and Wirtz, D., 2010, “A Distinctive Role for Focal Adhesion Proteins in Three-Dimensional Cell Motility,” Nat. Cell Biol., 12(6), pp. 598–604. [CrossRef] [PubMed]
Legant, W. R., Miller, J. S., Blakely, B. L., Cohen, D. M., Genin, G. M., and Chen, C. S., 2010, “Measurement of Mechanical Tractions Exerted by Cells in Three-Dimensional Matrices,” Nat. Methods, 7(12), pp. 969–971. [CrossRef] [PubMed]
Khetan, S., Guvendiren, M., Legant, W. R., Cohen, D. M., Chen, C. S., and Burdick, J. A., 2013, “Degradation-Mediated Cellular Traction Directs Stem Cell Fate in Covalently Crosslinked Three-Dimensional Hydrogels,” Nat. Mater, 12(5), pp. 458–465. [CrossRef] [PubMed]
Kutys, M. L., and Yamada, K. M., 2014, “An Extracellular-Matrix-Specific Gef-Gap Interaction Regulates Rho GTPase Crosstalk for 3D Collagen Migration,” Nat. Cell Biol., 16(9), pp. 909–917. [CrossRef] [PubMed]
Petrie, R. J., Koo, H., and Yamada, K. M., 2014, “Generation of Compartmentalized Pressure by a Nuclear Piston Governs Cell Motility in a 3D Matrix,” Science, 345(6200), pp. 1062–1065. [CrossRef] [PubMed]
Wu, P. H., Giri, A., Sun, S. X., and Wirtz, D., 2014, “Three-Dimensional Cell Migration Does Not Follow a Random Walk,” Proc. Natl. Acad. Sci. U. S. A., 111(11), pp. 3949–3954. [CrossRef] [PubMed]
Koch, T. M., Munster, S., Bonakdar, N., Butler, J. P., and Fabry, B., 2012, “3D Traction Forces in Cancer Cell Invasion,” PLoS One, 7(3), p. e33476. [CrossRef] [PubMed]
Kraning-Rush, C. M., Carey, S. P., Califano, J. P., Smith, B. N., and Reinhart-King, C. A., 2011, “The Role of the Cytoskeleton in Cellular Force Generation in 2D and 3D Environments,” Phys. Biol., 8(1), p. 015009. [CrossRef] [PubMed]
Campas, O., Mammoto, T., Hasso, S., Sperling, R. A., O’connell, D., Bischof, A. G., Maas, R., Weitz, D. A., Mahadevan, L., and Ingber, D. E., 2014, “Quantifying Cell-Generated Mechanical Forces Within Living Embryonic Tissues,” Nat. Methods, 11(2), pp. 183–189. [CrossRef] [PubMed]
Legant, W. R., Choi, C. K., Miller, J. S., Shao, L., Gao, L., Betzig, E., and Chen, C. S., 2013, “Multidimensional Traction Force Microscopy Reveals out-of-Plane Rotational Moments About Focal Adhesions,” Proc. Natl. Acad. Sci. U. S. A., 110(3), pp. 881–886. [CrossRef] [PubMed]
Fraley, S. I., Feng, Y. F., Wirtz, D., and Longmore, G. D., 2011, “Reply: Reducing Background Fluorescence Reveals Adhesions in 3D Matrices,” Nat. Cell Biol., 13(1), pp. 3–5. [CrossRef] [PubMed]
Mason, B. N., and Reinhart-King, C. A., 2013, “Controlling the Mechanical Properties of Three-Dimensional Matrices via Non-Enzymatic Collagen Glycation,” Organogenesis, 9(2), pp. 70–75. [CrossRef] [PubMed]
Mason, B. N., Starchenko, A., Williams, R. M., Bonassar, L. J., and Reinhart-King, C. A., 2013, “Tuning Three-Dimensional Collagen Matrix Stiffness Independently of Collagen Concentration Modulates Endothelial Cell Behavior,” Acta Biomater., 9(1), pp. 4635–4644. [CrossRef] [PubMed]
Salimath, A. S., Phelps, E. A., Boopathy, A. V., Che, P. L., Brown, M., Garcia, A. J., and Davis, M. E., 2012, “Dual Delivery of Hepatocyte and Vascular Endothelial Growth Factors via a Protease-Degradable Hydrogel Improves Cardiac Function in Rats,” PLoS One, 7(11), p. e50980. [CrossRef] [PubMed]




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