A Novel Cell Traction Force Microscopy to Study Multi-Cellular System

PLoS Computational Biology

Volumn 10, Issue 6, 2014, Pages

  Tang, Xin ^a   Tofangchi, Alireza ^a   Anand, Sandeep V ^a   Saif, Taher A ^a,b  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; FINITE ELEMENT METHOD; SUBSTRATES; TRACTION (FRICTION);

ACCURATE QUANTIFICATIONS; ADHERENT CELLS; CELL CLUSTERS; CELL TRACTION FORCE; CELLULAR FUNCTION; CELLULAR SYSTEM; MECHANISTICS; MICROENVIRONMENTS; TRACTION FORCE MICROSCOPIES; TRACTION FORCES;

CELLS;

POLYACRYLAMIDE GEL;

ANIMAL CELL; ARTICLE; ARTIFICIAL MEMBRANE; CANCER CELL LINE; CELL INTERACTION; CELL ISOLATION; CELL SIZE; CELLULAR PARAMETERS; CELLULAR TRACTION FORCE; CLUSTER ANALYSIS; COMPRESSION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DIGITAL IMAGING; DIPOLE; ELASTICITY; ELECTRON MICROSCOPY; FIBROBLAST; FINITE ELEMENT ANALYSIS; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MECHANOTRANSDUCTION; MICROENVIRONMENT; NONHUMAN; QUANTITATIVE STUDY; THREE DIMENSIONAL IMAGING; TRACTION FORCE MICROSCOPY; VALIDATION STUDY; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; BIOPHYSICS; CELL ADHESION; CELL CULTURE; COMPRESSIVE STRENGTH; MICROSCOPY; PHYSIOLOGY; PROCEDURES; TENSILE STRENGTH; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANIMALS; BIOPHYSICAL PHENOMENA; CELL ADHESION; CELL LINE, TUMOR; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; COMPRESSIVE STRENGTH; COMPUTATIONAL BIOLOGY; FINITE ELEMENT ANALYSIS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICROSCOPY; MODELS, BIOLOGICAL; TENSILE STRENGTH;

EID: 84903388927     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003631     Document Type: Article

References (112)

1. Bischofs IB, Schwarz US, (2003) Cell organization in soft media due to active mechanosensing. Proc Natl Acad Sci USA 100: 9274-9279.
2. De R, Zemel A, Safran SA, (2007) Dynamics of cell orientation. Nature Physics 3: 655-659.
3. Friedrich BM, Buxboim A, Discher DE, Safran SA, (2011) Striated Acto-Myosin Fibers Can Reorganize and Register in Response to Elastic Interactions with the Matrix. Biophysical Journal 100: 2706-2715.
4. Reinhart-King CA, Dembo M, Hammer DA, (2008) Cell-Cell Mechanical Communication through Compliant Substrates. Biophysical Journal 95: 6044-6051.
5. Nicolas A, Besser A, Safran SA, (2008) Dynamics of Cellular Focal Adhesions on Deformable Substrates: Consequences for Cell Force Microscopy. Biophysical Journal 95: 527-539.
6. Zhou EH, Trepat X, Park CY, Lenormand G, Oliver MN, et al. (2009) Universal behavior of the osmotically compressed cell and its analogy to the colloidal glass transition. Proc Natl Acad Sci USA 10610632-1-637.
7. Tang X, Kuhlenschmidt TB, Zhou J, Bell P, Wang F, et al. (2010) Mechanical force affects expression of an in vitro metastasis-like phenotype in HCT-8 cells. Biophysics 99: 2460-2469.
8. Tang X, Cappa T, Kuhlenschmidt T, Kuhlenschmidt M, Saif T (2011) Mechanobiology of Cell-Cell and Cell-Matrix Interactions. In: Johnson AW, Harley B, editors. Specific and Non-Specific Adhesion in Cancer Cells with Various Metastatic Potentials: Springer Science.
9. Sheetz M, Vogel V, (2006) Local force and geometry sensing regulate cell functions. Nature Revuews Molecular Cell Biology 7: 265-275.
10. Schwarz US, (2007) Soft matters in cell adhesion: rigidity sensing on soft elastic substrates. Soft Matter 3: 263-266.
11. Tang X, Bajaj P, Bashir R, Saif T, (2011) How far cardiac cells can see each other mechanically. Soft Matter 7: 6151-6158.
12. Discher DE, Janmey P, Wang YL, (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-1143.
13. Bajaj P, Tang X, Saif TA, Bashir R, (2010) Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes. Journal of Biomedical Materials Research Part A 95: 1261-1269.
14. Eyckmans J, Boudou T, Yu X, Chen CS, (2011) A Hitchhiker's Guide to Mechanobiology. Developmental Cell 21: 35-47.
15. Geiger B, Bershadsky A, (2002) Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell 110: 139-142.
16. Cukierman E, Pankov R, Stevens D, Yamada K, (2001) Taking cell-matrix adhesions to the third dimension. Science 294: 1708-1712.
17. Yang J, Rayburn H, Hynes R, (1995) Cell-adhesion events mediated by alpha(4) integrins are essential in placental and cardiac development. Development** 121: 549-560.
18. Zemel A, Rehfeldt F, Brown AEX, Discher DE, Safran SA, (2010) Cell shape, spreading symmetry, and the polarization of stress-fibers in cells. Journal of Physics: Condensed Matter 22: 194110-194130.
19. Even-Ram S, Yamada K, (2005) Cell migration in 3d matrix. Current Opinion in Cell Biology 17: 524-532.
20. Doyle A, Marganski W, Lee J, (2004) Calcium transients induce spatially coordinated increases in traction force during the movement of fish keratocytes. Journal of Cell Science 117: 2203-2214.
21. Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang H-Y, et al. (2008) Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. Journal of Cell Science 121: 3794-3802.
22. Engler AJ, Sen S, Sweeney HL, Discher DE, (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
23. Galbraith C, Yamada K, Sheetz M, (2002) The relationship between force and focal complex development. Cell Biology 159: 695-705.
24. Georges PC, Janmey PA, (2005) Cell type-specific response to growth on soft materials. Journal of Applied Physiology 98: 1547-1553.
25. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, et al. (2009) Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling. Cell 139: 891-906.
26. Lo C-M, Wang H-B, Dembo M, Wang Y-l, (2000) Cell Movement Is Guided by the Rigidity of the Substrate. Biophysical Journal 79: 144-152.
27. Eisenberg JL, Safi A, Wei X, Espinosa HD, Budinger GS, et al. (2011) Substrate stiffness regulates extracellular matrix deposition by alveolar epithelial cells. Research and Reports in Biology 2: 1-12.
28. Tang X, Qi W, Kuhlenschmidt T, Kuhlenschmidt M, Janmey P, et al. (2012) Attenuation of Cell Mechano-sensitivity in Colon Cancer Cells during in vitro Metastasis. PlosONE 7: e50443.
29. Tang X, Kuhlenschmidt TB, Li Q, Ali S, Lezmi S, et al. (2014) A Mechanically-induced Colon Cancer Cell Population Shows Increased Metastatic Potential. Molecular Cancer: In press.
30. Tang X, Cappa T, Kuhlenschmidt TB, Kuhlenschmidt MS, Saif TA, (2010) Studying the Mechanical Sensitivity of Human Colon Cancer Cells Through a Novel Bio-MEMS Force Sensor. ASME 2010 First Global Congress on NanoEngineering for Medicine and Biology NEMB2010-13237 pp. 45-46.
31. Tang X, Saif TA, (2013) Adhesivity of Colon Cancer Cells during in vitro Metastasis. International Journal of Applied Mechanics 5: 1350025.
32. Zemel A, Rehfeldt F, Brown AEX, Discher DE, Safran SA, (2010) Optimal matrix rigidity for stress fiber polarization in stem cells. Nature Physics 1: 468-473.
33. Beningo KA, Dembo M, Kaverina I, Small JV, Wang Y-l, (2001) Nascent Focal Adhesions Are Responsible for the Generation of Strong Propulsive Forces in Migrating Fibroblasts. The Journal of Cell Biology 153: 881-887.
34. Reinhart-King CA, Dembo M, Hammer DA, (2005) The Dynamics and Mechanics of Endothelial Cell Spreading. Biophysical Journal 89: 676-689.
35. Rajagopalan J, Tofangchi A, Saif MTA, (2010) Drosophila Neurons Actively Regulate Axonal Tension In Vivo. Biophysical journal 99: 3208-3215.
36. Leckband DE, Duc Ql, Wang N, Rooij Jd, (2011) Mechanotransduction at cadherin-mediated adhesions. Current Opinion in Cell Biology 23: 523-530.
37. Chen CS, Tan J, Tien J, (2004) Mechanotransduction at cell-matrix and cell-cell contacts. Annual Review of Biomedical Engineering 6: 275-302.
38. Bao G, Kamn RD, Thomas W, Wonmuk Hwang DAF, Grodzinsky AJ, et al. (2010) Molecular Biomechanics: The Molecular Basis of How Forces Regulate Cellular Function. Cellular and Molecular Bioengineering 3: 91-105.
39. Wang J, Lin J, (2007) Cell traction force and measurement methods. Biomechanics and Modeling in Mechanobiology 6: 361-371.
40. Wang JH-C, Li B (2010) The principles and biological applications of cell traction force microscopy Microscopy: Science, Technology, Applications and Education: 449-458.
41. Beningo KA, Wang Y-L, (2002) Flexible substrata for the detection of cellular traction forces. TRENDS in Cell Biology 12: 79-84.
42. Rajagopalan J, Saif MTA, (2011) MEMS Sensors and Microsystems for Cell Mechanobiology. Journal of Micromechanics and Microengineering 21: 1-11.
43. Pruitt BL, Herr AE, (2011) MEMS in biology and medicine. Journal of Micromechanics and Microengineering 21: 1-2.
44. Rajagopalan J, Tofangchi A, Saif MTA, (2010) Linear High-Resolution BioMEMS Force Sensors With Large Measurement Range. Journal of Microelectromechanical Systems 19: 1380-1389.
45. Harris AK, Wild P, Stopak D, (1980) Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208(4440): 177-179.
46. Lee J, Leonard M, Oliver T, Ishihara A, Jacobson K, (1994) Traction forces generated by locomoting keratocytes. Cell Biology 127: 1957-1964.
47. Oliver T, Dembo M, Jacobson K, (1995) Traction forces in locomoting cells. Cell Motil Cytoskeleton * 31: 225-240.
48. Dembo M, Oliver T, Ishihara A, Jacobson K, (1996) Imaging the traction stresses exerted by locomoting cells with the elastic substratum method. Biophysics 70: 2008-2022.
49. Butler JP, Tolic-Norrelykke IM, Fabry B, Fredberg JJ, (2002) Traction fields, moments, and strain energy that cells exert on their surroundings. American Journal of Physiology Cell Physiology 282: C595-C605.
50. Schwarz US, Balaban NQ, Riveline D, Bershadsky A, Geiger B, Safran SA, (2002) Calculation of forces at focal adhesions from elastic substrate data: the effect of localized force and the need for regularization. Biophysics 83(3): 1380-1394.
51. Dembo M, Wang Y, (1999) Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophysics 76: 2307-2316.
52. Schwarz U, Balaban N, Riveline D, Addadi L, Bershadsky A, et al. (2003) Measurement of cellular forces at focal adhesions using elastic micro-patterned substrates. Mat Science Engin C-Biom and Supramol Syst ** 23: 387-394.
53. Huang J, Qin L, Peng X, Zhu T, Xiong C, et al. (2009) Cellular traction force recovery: An optimal filtering approach in two-dimensional Fourier space. Journal of Theoretical Biology 259: 811-819.
54. Harley BA, Freyman TM, Wong MQ, Gibson LJ, (2007) A New Technique for Calculating Individual Dermal Fibroblast Contractile Forces Generated within Collagen-GAG Scaffolds. Biophysical Journal 93: 2911-2922.
55. Marganski WA, Dembo M, Wang YL, (2003) Measurements of cell-generated deformations on flexible substrata using correlation-based optical flow. Methods in Enzymology 361: 197-211.
56. Yang Z, Lin J-S, Chen J, Wang JH-C, (2006) Determining substrate displacement and cell traction fields- a new approach. Journal of Theoretical Biology 242: 607-616.
57. Landau LD, Lifshitz EM, Kosevich AM, Pitaevski LP (1995) Theory of Elasticity. Pergamon Press, Oxford. pp. 25-37.
58. Munevar S, Wang Y-l, Dembo M, (2001) Traction Force Microscopy of Migrating Normal and H-ras Transformed 3T3 Fibroblasts. Biophysical Journal 80: 1744-1757.
59. Beningo KA, Dembo M, Wang Y-l, (2004) Responses of fibroblasts to anchorage of dorsal extracellular matrix receptors. Proc Natl Acad Sci USA 101: 18024-18029.
60. Tambe DT, Hardin CC, Angelini TE, Rajendran K, Park CY, et al. (2011) Collective cell guidance by cooperative intercellular forces. Nature Materials 10: 469-475.
61. Lin Y-C, Tambe DT, Park CY, Wasserman MR, Trepat X, et al. (2010) Mechanosensing of substrate thickness. Physical Review E 82: 041918 (041916).
62. Serra-Picamal X, Conte V, Vincent R, Anon E, Tambe DT, et al. (2012) Mechanical waves during tissue expansion. Nature Physics 8: 628-634.
63. Trepat X, Wasserman MR, Angelini TE, Millet E, Weitz DA, et al. (2009) Physical forces during collective cell migration. Nature Physics 5: 426-430.
64. Scrimgeour J, Kodali VK, Kovari DT, Curtis JE, (2010) Photobleaching-activated micropatterning on self-assembled monolayers. Journal of Physics: Condensed Matter 22: 194103.
65. Stricker J, Sabass B, Schwarz US, Gardel ML, (2010) Optimization of traction force microscopy for micron-sized focal adhesions. Journal of Physics: Condensed Matter 22: 194104.
66. Ng SS, Li C, Chan V, (2011) Experimental and numerical determination of cellular traction force on polymeric hydrogels. Interface Focus 1: 777-791.
67. Huang J, Peng X, Qin L, Zhu T, Xiong C, et al. (2009) Determination of cellular tractions on elastic substrate based on an integral boussinesq solution. ASME Journal of Biomechanical Engineering 131: 061009.
68. Zaman M KR, Matsudaira P, Lauffenburger D, (2005) Computational model for cell migration in three-dimensional matrices. Biophysics 89: 1389-1397.
69. Hur S, Zhao Y, Li YS, Botvinick E, Chien S, (2009) Live cells exert 3-dimensional traction forces on their substrata. Cellular and Molecular Bioengineering 2: 425-436.
70. Franck C, Maskarinec S, Tirrell DA, Ravichandran G, (2011) Three-Dimensional Traction Force Microscopy: A New Tool for Quantifying Cell-Matrix Interactions. PLoS ONE 6(3): e17833.
71. Bloom RJ, George JP, Celedon A, Sun SX, Wirtz D, (2008) Mapping Local Matrix Remodeling Induced by a Migrating Tumor Cell Using Three-Dimensional Multiple-Particle Tracking. Biophysical Journal 95: 4077-4088.
72. Koch TM, Münster S, Bonakdar N, Butler JP, Fabry B, (2012) 3D Traction Forces in Cancer Cell Invasion. PLoS ONE 7(3): e33476.
73. Hall MS, Long R, Hui C-Y, Wu M, (2012) Mapping Three-Dimensional Stress and Strain Fields within a Soft Hydrogel Using a Fluorescence Microscope. Biophysical Journal 102: 2241-2250.
74. Ingber DE, (2006) Cellular mechanotransduction: putting all the pieces together again. The FASEB Journal 20: 811-827.
75. Lecuit T, Lenne PFo, (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nature Reviews Molecular Cell Biology 8: 633-644.
76. Guo C-L, Ouyang M, Yu J-Y, Price A, Maslov J, (2011) Long-range mechanical force in colony branching and tumor invasion. Proc of SPIE 8099: 809903-809901-809908.
77. Moore SW, Roca-Cusachs P, Sheetz MP, (2010) Stretchy Proteins on Stretchy Substrates: The Important Elements of Integrin-Mediated Rigidity Sensing. Developmental Cell 19: 194-206.
78. Levental I, Georges PC, Janmey PA, (2006) Soft biological materials and their impact on cell function. Soft Matter 3: 299-306.
79. Li D, Zhou J, Chowdhury F, Cheng J, Wang N, et al. (2012) Role of mechanical factors in fate decisions of stem cells. Regenerative Medicine 6: 229-240.
80. Wang Y-L, Pelham RJ Jr, (1998) Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol 298: 489-496.
81. Damljanovic V, Lagerholm BC, Jacobson K, (2005) Bulk and micropatterned conjugation of extracellular matrix proteins to characterized polyacrylamide substrates for cell mechanotransduction assays. Biotechniques 39: 847-851.
82. Tang X, Ali MY, Saif MTA, (2012) A Novel Technique for Micro-patterning Proteins and Cells on Polyacrylamide Gels. Soft Matter 8: 3197-3206.
83. Pelham R, Wang Y, (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proceeding of National Academy of Science in USA 94: 13661-13665.
84. Aratyn-Schaus Y, Oakes PW, Stricker J, Winter SP, Gardel ML, (2010) Preparation of Complaint Matrices for Quantifying Cellular Contraction. Journal of Visualized Experiments 46: e2173.
85. Cha C, Jeong JH, Tang X, Zill AT, Prakash YS, et al. (2011) Top-down synthesis of versatile polyaspartamide linkers for single-step protein conjugation to materials. Bioconjugate Chemistry 22: 2377-2382.
86. Li H, Guo X, Nuzzo RG, Hsia J, (2010) Capillary induced self-assembly of thin foils into 3D structures. Journal of the Mechanics and Physics of Solids 58: 2033-2042.
87. Engler AJ, Rehfeldt F, Sen S, Disher DE, (2007) Microtissue elasticity: measurements by Atomic Force Microscopy and its influence on cell differentiation. Methods in cell biology 83: 521-545.
88. Dong R, Jensen TW, Engberg K, Nuzzo RG, Leckband DE, (2007) Variably elastic hydrogel patterned via capillary action in microchannels. Langmuir 23: 1483-1488.
89. Minary-Jolandan M, Yu M-F, (2009) Nanomechanical Heterogeneity in the Gap and Overlap Regions of Type I Collagen Fibrils with Implications for Bone Heterogeneity. Biomacromolecules 10: 2565-2570.
90. Vendroux G, Knauss WG, (1998) Submicron Deformation Field Measurements II Improved Digital Image Correlation. Experimental Mechanics 38: 86-92.
91. Sutton MA, Wolters WJ, Peters WH, Ranson M, McNeil SR, (1983) Determination of Displacements Using an Improved Digital Image Correlation Method. Image Vision Computing 1: 133-139.
92. Sutton MA, McNeill SR, Helm JD, Chao YJ, (2000) Advances in Two-Dimensional and Three-Dimensional Computer Vision. Photomechanics 77: 323-372.
93. Huang J, Zhu T, Pan X, Qin L, Peng X, et al. (2010) A high-efficiency digital image correlation method based on a fast recursive scheme. Measurement Science and Technology 21: 1-12.
94. Eberl C, Gianola DS, Thompson R (2006) MatLab Central (Natick, MA: The Mathworks, Inc., 2006).
95. Pan B, Xie H, Wang Z, Qian K, Wang Z, (2008) Study on subset size selection in digital image correlation for speckle patterns. Optics Express 16: 7037-7048.
96. Pan B, Qian K, Xie H, Asundi A (2009) Two-dimensional digital image correlation for in-plane displacement and strain measurement: a review. Measurement science and technology 20.
97. Correlated Solutions I (2009) Vic 2D. Columbia.
98. Mal AK, Singh SJ (1991) Deformation of elastic solids: New Jersey: Prentice Hall.
99. Storm C, Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA, (2005) Nonlinear elasticity in biological gels. Nature 435: 191-194.
100. Fung Y-C, Tong P (2001) Classical and Computational Solid Mechanics: World Scientific Publishing Company.
101. Fung Y-C (1993) A First Course in Continuum Mechanics: Prentice Hall.
102. Trepat X, Fredberg JJ, (2011) Plithotaxis and emergent dynamics in collective cellular migration. Trends in Cell Biology 812: 1-9.
103. Sheetz M, Vogel V, (2006) Local force and geometry sensing regulate cell functions. Nature Reviews Molecular Cell Biology 7: 265-275.
104. Ingber DE, (2006) The FASEB Journal Cellular mechanotransduction: putting all the pieces together again. 20: 811-827.
105. Humphrey JD, (2003) Continuum biomechanics of soft biological tissues. Proceeding of Royal Society of London 459: 3-46.
106. Guo Z, Vita RD, (2009) Probabilistic Constitutive Law for Damage in Ligaments. Medical Engineering & Physics 31: 1104-1109.
107. Maloney JM, Walton EB, Bruce CM, Vliet KJV, (2008) Influence of finite thickness and stiffness on cellular adhesion-induced deformation of compliant substrata. Physical Review E 78: 041923 (041915).
108. Harjanto D, Zaman MH, (2010) Matrix mechanics and receptor-ligand interactions in cell adhesion. Organic & Biomolecular Chemistry 8: 299-304.
109. Buxboim A, Ivanovska IL, Discher DE, (2010) Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in? Journal of Cell Science 123: 297-308.
110. Winer JP, Oake S, Janmey PA, (2009) Non-Linear Elasticity of Extracellular Matrices Enables Contractile Cells to Communicate Local Position and Orientation. PLoS ONE 4: e6382.
111. Ricart BG, Yang MT, Hunter CA, Chen CS, Hammer DA, (2011) Measuring Traction Forces of Motile Dendritic Cells on Micropost Arrays. Biophysical Journal 101: 2620-2628.
112. Ghibaudo M, Saez A, Trichet La, Xayaphoummine A, Browaeys J, et al. (2008) Traction forces and rigidity sensing regulate cell functions. Soft Matter 4: 1836-1843.