Multiscale mechanobiology: Computational models for integrating molecules to multicellular systems

Integrative Biology (United Kingdom)

Volumn 7, Issue 10, 2015, Pages 1093-1108

  Mak, Michael ^a,b   Kim, Taeyoon ^c   Zaman, Muhammad H ^b   Kamm, Roger D ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b Boston University   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN FILAMENT; BIOLOGY; CELL MOTION; CELLS; CYTOSKELETON; EXTRACELLULAR MATRIX; FORCE; MECHANICS; MECHANOTRANSDUCTION; MOLECULE; MULTICELLULAR SYSTEM; MULTISCALE MECHANOBIOLOGY; PRIORITY JOURNAL; PROTEIN UNFOLDING; REVIEW; RIGIDITY; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; BIOPHYSICS; CELL COMMUNICATION; COMPUTER SIMULATION; HUMAN; MOLECULAR DYNAMICS; PHYSIOLOGY; SYSTEMS BIOLOGY;

MOLECULAR MOTOR;

ACTIN CYTOSKELETON; ANIMALS; BIOMECHANICAL PHENOMENA; BIOPHYSICS; CELL COMMUNICATION; COMPUTER SIMULATION; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; MOLECULAR DYNAMICS SIMULATION; MOLECULAR MOTOR PROTEINS; SYSTEMS BIOLOGY;

EID: 84943389596     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c5ib00043b     Document Type: Review

References (139)

1. J. C. Phillips R. Braun W. Wang J. Gumbart E. Tajkhorshid E. Villa C. Chipot R. D. Skeel L. Kalé K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 2005 26 1781 1802
2. V. P. Hytönen V. Vogel How Force Might Activate Talin's Vinculin Binding Sites: SMD Reveals a Structural Mechanism PLoS Comput. Biol. 2008 4 e24
3. K. S. Kolahi M. R. K. Mofrad Molecular Mechanics of Filamin's Rod Domain Biophys. J. 2008 94 1075 1083
4. T. Kim W. Hwang H. Lee R. D. Kamm Computational analysis of viscoelastic properties of crosslinked actin networks PLoS Comput. Biol. 2009 5 e1000439
5. B. Szabó G. J. Szöllösi B. Gönci Z. Jurányi D. Selmeczi T. Vicsek Phase transition in the collective migration of tissue cells: experiment and model Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 2006 74 061908
6. N. Sepúlveda L. Petitjean O. Cochet E. Grasland-Mongrain P. Silberzan V. Hakim Collective Cell Motion in an Epithelial Sheet Can Be Quantitatively Described by a Stochastic Interacting Particle Model PLoS Comput. Biol. 2013 9 e1002944
7. L. Zhang C. A. Athale T. S. Deisboeck Development of a three-dimensional multiscale agent-based tumor model: Simulating gene-protein interaction profiles, cell phenotypes and multicellular patterns in brain cancer J. Theor. Biol. 2007 244 96 107
8. J. D. Humphrey Review Paper: Continuum biomechanics of soft biological tissues Proc. R. Soc. London, Ser. A 2003 459 3 46
9. S. A. Maas B. J. Ellis G. A. Ateshian J. A. Weiss FEBio: Finite Elements for Biomechanics J. Biomech. Eng. 2012 134 011005
10. C. T. Lim E. H. Zhou S. T. Quek Mechanical models for living cells - a review J. Biomech. 2006 39 195 216
11. N. B. Ouchi J. A. Glazier J.-P. Rieu A. Upadhyaya Y. Sawada Improving the realism of the cellular Potts model in simulations of biological cells Phys. A 2003 329 451 458
12. E. Boghaert D. C. Radisky C. M. Nelson Lattice-Based Model of Ductal Carcinoma In Situ Suggests Rules for Breast Cancer Progression to an Invasive State PLoS Comput. Biol. 2014 10 e1003997
13. R. F. M. van Oers E. G. Rens D. J. LaValley C. A. Reinhart-King R. M. H. Merks Mechanical Cell-Matrix Feedback Explains Pairwise and Collective Endothelial Cell Behavior In Vitro PLoS Comput. Biol. 2014 10 e1003774
14. C. Bustamante Z. Bryant S. B. Smith Ten years of tension: single-molecule DNA mechanics Nature 2003 421 423 427
15. A. del Rio R. Perez-Jimenez R. Liu P. Roca-Cusachs J. M. Fernandez M. P. Sheetz Stretching Single Talin Rod Molecules Activates Vinculin Binding Science 2009 323 638 641
16. V. Vogel Mechanotransduction Involving Multimodular Proteins: Converting Force into Biochemical Signals Annu. Rev. Biophys. Biomol. Struct. 2006 35 459 488
17. I. Schoen B. L. Pruitt V. Vogel The Yin-Yang of Rigidity Sensing: How Forces and Mechanical Properties Regulate the Cellular Response to Materials Annu. Rev. Mater. Res. 2013 43 589 618
18. H. S. Chen K. S. Kolahi M. R. K. Mofrad Phosphorylation Facilitates the Integrin Binding of Filamin under Force Biophys. J. 2009 97 3095 3104
19. L. Rognoni T. Möst G. Žoldák M. Rief Force-dependent isomerization kinetics of a highly conserved proline switch modulates the mechanosensing region of filamin Proc. Natl. Acad. Sci. U. S. A. 2014 111 5568 5573
20. J. Yan M. Yao B. Goult M. Sheetz Talin Dependent Mechanosensitivity of Cell Focal Adhesions Cell. Mol. Bioeng. 2014 1 9
21. S. E. Lee S. Chunsrivirot R. D. Kamm M. R. K. Mofrad Molecular Dynamics Study of Talin-Vinculin Binding Biophys. J. 2008 95 2027 2036
22. M. Yao B. T. Goult H. Chen P. Cong M. P. Sheetz J. Yan Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation Sci. Rep. 2014 4 10.1038/srep04610
23. F. Margadant L. L. Chew X. Hu H. Yu N. Bate X. Zhang M. Sheetz Mechanotransduction In Vivo by Repeated Talin Stretch-Relaxation Events Depends upon Vinculin PLoS Biol. 2011 9 e1001223
24. A. Nicolas B. Geiger S. A. Safran Cell mechanosensitivity controls the anisotropy of focal adhesions Proc. Natl. Acad. Sci. U. S. A. 2004 101 12520 12525
25. H. Shams J. Golji M. R. K. Mofrad A Molecular Trajectory of α-Actinin Activation Biophys. J. 2012 103 2050 2059
26. B. Martinac Mechanosensitive ion channels: molecules of mechanotransduction J. Cell Sci. 2004 117 2449 2460
27. F. Kong A. J. García A. P. Mould M. J. Humphries C. Zhu Demonstration of catch bonds between an integrin and its ligand J. Cell Biol. 2009 185 1275 1284
28. W. E. Thomas V. Vogel E. Sokurenko Biophysics of Catch Bonds Annu. Rev. Biophys. 2008 37 399 416
29. C. Storm J. J. Pastore F. C. MacKintosh T. C. Lubensky P. A. Janmey Nonlinear elasticity in biological gels Nature 2005 435 191 194
30. T. C. Bidone T. Kim M. A. Deriu U. Morbiducci R. D. Kamm Multiscale impact of nucleotides and cations on the conformational equilibrium, elasticity and rheology of actin filaments and crosslinked networks Biomech. Model. Mechanobiol. 2015 10.1007/s10237-015-0660-6
31. M. L. Gardel J. H. Shin F. C. MacKintosh L. Mahadevan P. Matsudaira D. A. Weitz Elastic Behavior of Cross-Linked and Bundled Actin Networks Science 2004 304 1301 1305
32. P. R. Onck T. Koeman T. van Dillen E. van der Giessen Alternative Explanation of Stiffening in Cross-Linked Semiflexible Networks Phys. Rev. Lett. 2005 95 178102
33. A.-X. Zhou J. H. Hartwig L. M. Akyürek Filamins in cell signaling, transcription and organ development Trends Cell Biol. 2010 20 113 123
34. J. Stricker T. Falzone M. L. Gardel Mechanics of the F-actin cytoskeleton J. Biomech. 2010 43 9 14
35. N. Wang J. D. Tytell D. E. Ingber Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus Nat. Rev. Mol. Cell Biol. 2009 10 75 82
36. M. R. K. Mofrad Rheology of the Cytoskeleton Annu. Rev. Fluid Mech. 2009 41 433 453
37. M. J. Unterberger G. A. Holzapfel Advances in the mechanical modeling of filamentous actin and its cross-linked networks on multiple scales Biomech. Model. Mechanobiol. 2014 13 1155 1174
38. M. L. Gardel K. E. Kasza C. P. Brangwynne J. Y. Liu D. A. Weitz Mechanical Response of Cytoskeletal Networks Methods Cell Biol. 2008 89 487 519
39. K. M. Schmoller O. Lieleg A. R. Bausch Structural and Viscoelastic Properties of Actin/Filamin Networks: Cross-Linked versus Bundled Networks Biophys. J. 2009 97 83 89
40. R. Tharmann M. M. A. E. Claessens A. R. Bausch Micro- and macrorheological properties of actin networks effectively cross-linked by depletion forces Biophys. J. 2006 90 2622 2627
41. M. L. Gardel F. Nakamura J. H. Hartwig J. C. Crocker T. P. Stossel D. A. Weitz Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells Proc. Natl. Acad. Sci. U. S. A. 2006 103 1762 1767
42. B. Wagner R. Tharmann I. Haase M. Fischer A. R. Bausch Cytoskeletal polymer networks: the molecular structure of cross-linkers determines macroscopic properties Proc. Natl. Acad. Sci. U. S. A. 2006 103 13974 13978
43. E. M. Huisman T. van Dillen P. R. Onck E. Van der Giessen Three-dimensional cross-linked F-actin networks: Relation between network architecture and mechanical behavior Phys. Rev. Lett. 2007 99 208103
44. O. Chaudhuri S. H. Parekh D. A. Fletcher Reversible stress softening of actin networks Nature 2007 445 295 298
45. T. Wu J. J. Feng A Biomechanical Model for Fluidization of Cells under Dynamic Strain Biophys. J. 2015 108 43 52
46. C. Chen R. Krishnan E. Zhou A. Ramachandran D. Tambe K. Rajendran R. M. Adam L. Deng J. J. Fredberg Fluidization and Resolidification of the Human Bladder Smooth Muscle Cell in Response to Transient Stretch PLoS One 2010 5 e12035
47. T. Kim W. Hwang R. D. Kamm Dynamic Role of Cross-Linking Proteins in Actin Rheology Biophys. J. 2011 101 1597 1603
48. J. A. Astrom P. B. S. Kumar I. Vattulainen M. Karttunen Strain hardening, avalanches, and strain softening in dense cross-linked actin networks Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 2008 77 051913
49. A. S. Abhilash P. K. Purohit S. P. Joshi Stochastic rate-dependent elasticity and failure of soft fibrous networks Soft Matter 2012 8 7004 7016
50. T. Li D. Hu P. K. D. V. Yarlagadda Y. Gu Physical mechanism of the compressive response of F-actin networks: significance of crosslinker unbinding events Theor. Appl. Mech. Lett. 2014 4 051006
51. P. S. P. Silveira A. M. Alencar A. Majumdar M. Lemos J. J. Fredberg B. Suki Percolation in a network with long-range connections: Implications for cytoskeletal structure and function Physica A 2009 388 1521 1526
52. C. P. Broedersz X. M. Mao T. C. Lubensky F. C. MacKintosh Criticality and isostaticity in fibre networks Nat. Phys. 2011 7 983 988
53. C. J. Cyron K. W. M. ller K. M. Schmoller A. R. Bausch W. A. Wall R. F. Bruinsma Equilibrium phase diagram of semi-flexible polymer networks with linkers EPL 2013 102 38003
54. F. C. MacKintosh C. F. Schmidt Active cellular materials Curr. Opin. Cell Biol. 2010 22 29 35
55. M. Schliwa G. Woehlke Molecular motors Nature 2003 422 759 765
56. D. Mizuno C. Tardin C. F. Schmidt F. C. MacKintosh Nonequilibrium mechanics of active cytoskeletal networks Science 2007 315 370 373
57. G. H. Koenderink Z. Dogic F. Nakamura P. M. Bendix F. C. MacKintosh J. H. Hartwig T. P. Stossel D. A. Weitz An active biopolymer network controlled by molecular motors Proc. Natl. Acad. Sci. U. S. A. 2009 106 15192 15197
58. C. P. Broedersz F. C. MacKintosh Molecular motors stiffen non-affine semiflexible polymer networks Soft Matter 2011 7 3186 3191
59. N. L. Dasanayake P. J. Michalski A. E. Carlsson General Mechanism of Actomyosin Contractility Phys. Rev. Lett. 2011 107 118101
60. S. Wang P. G. Wolynes Active contractility in actomyosin networks Proc. Natl. Acad. Sci. U. S. A. 2012 109 6446 6451
61. J. Alvarado M. Sheinman A. Sharma F. C. MacKintosh G. H. Koenderink Molecular motors robustly drive active gels to a critically connected state Nat. Phys. 2013 9 591 597
62. J. A. Astrom P. B. S. Kumar M. Karttunen Aster formation and rupture transition in semi-flexible fiber networks with mobile cross-linkers Soft Matter 2009 5 2869 2874
63. C. Borau T. Kim T. Bidone J. M. García-Aznar R. D. Kamm Dynamic mechanisms of cell rigidity sensing: insights from a computational model of actomyosin networks PLoS One 2012 7 e49174
64. H. Parameswaran K. R. Lutchen B. Suki A computational model of the response of adherent cells to stretch and changes in substrate stiffness J. Appl. Physiol. 2014 116 825 834
65. J. Étienne J. Fouchard D. Mitrossilis N. Bufi P. Durand-Smet A. Asnacios Cells as liquid motors: Mechanosensitivity emerges from collective dynamics of actomyosin cortex Proc. Natl. Acad. Sci. U. S. A. 2015 112 2740 2745
66. A. Ward F. Hilitski W. Schwenger D. Welch A. W. C. Lau V. Vitelli L. Mahadevan Z. Dogic Solid friction between soft filaments Nat. Mater. 2015 14 583 588
67. Z. Liu J. L. Tan D. M. Cohen M. T. Yang N. J. Sniadecki S. A. Ruiz C. M. Nelson C. S. Chen Mechanical tugging force regulates the size of cell-cell junctions Proc. Natl. Acad. Sci. U. S. A. 2010 107 9944 9949
68. M. Behrndt C.-P. Heisenberg Lateral junction dynamics lead the way out Nat. Cell Biol. 2014 16 127 129
69. M. J. Paszek N. Zahir K. R. Johnson J. N. Lakins G. I. Rozenberg A. Gefen C. A. Reinhart-king S. S. Margulies M. Dembo D. Boettiger D. A. Hammer V. M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 2005 8 241 254
70. M. A. Wozniak K. Modzelewska L. Kwong P. J. Keely Focal adhesion regulation of cell behavior Biochim. Biophys. Acta, Mol. Cell Res. 2004 1692 103 119
71. I. Indra S. Hong R. Troyanovsky B. Kormos S. Troyanovsky The Adherens Junction: A Mosaic of Cadherin and Nectin Clusters Bundled by Actin Filaments J. Invest. Dermatol. 2013 133 2546 2554
72. M. J. Paszek D. Boettiger V. M. Weaver D. A. Hammer Integrin Clustering Is Driven by Mechanical Resistance from the Glycocalyx and the Substrate PLoS Comput. Biol. 2009 5 e1000604
73. M. J. Paszek C. C. DuFort O. Rossier R. Bainer J. K. Mouw K. Godula J. E. Hudak J. N. Lakins A. C. Wijekoon L. Cassereau M. G. Rubashkin M. J. Magbanua K. S. Thorn M. W. Davidson H. S. Rugo J. W. Park D. A. Hammer G. Giannone C. R. Bertozzi V. M. Weaver The cancer glycocalyx mechanically primes integrin-mediated growth and survival Nature 2014 511 319 325
74. Y. Jamali T. Jamali M. R. K. Mofrad An agent based model of integrin clustering: Exploring the role of ligand clustering, integrin homo-oligomerization, integrin-ligand affinity, membrane crowdedness and ligand mobility J. Comput. Phys. 2013 244 264 278
75. J. D. Humphrey E. R. Dufresne M. A. Schwartz Mechanotransduction and extracellular matrix homeostasis Nat. Rev. Mol. Cell Biol. 2014 15 802 812
76. C. L. Cummings D. Gawlitta R. M. Nerem J. P. Stegemann Properties of engineered vascular constructs made from collagen, fibrin, and collagen-fibrin mixtures Biomaterials 2004 25 3699 3706
77. K. Wolf M. te Lindert M. Krause S. Alexander J. te Riet A. L. Willis R. M. Hoffman C. G. Figdor S. J. Weiss P. Friedl Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force J. Cell Biol. 2013 201 1069 1084
78. D. Harjanto J. S. Maffei M. H. Zaman Quantitative Analysis of the Effect of Cancer Invasiveness and Collagen Concentration on 3D Matrix Remodeling PLoS One 2011 6 e24891
79. H. Wang A. S. Abhilash C. S. Chen R. G. Wells V. B. Shenoy Long-Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers Biophys. J. 2014 107 2592 2603
80. A. S. Abhilash B. M. Baker B. Trappmann C. S. Chen V. B. Shenoy Remodeling of Fibrous Extracellular Matrices by Contractile Cells: Predictions from Discrete Fiber Network Simulations Biophys. J. 2014 107 1829 1840
81. X. Ma M. E. Schickel M. D. Stevenson A. L. Sarang-Sieminski K. J. Gooch S. N. Ghadiali R. T. Hart Fibers in the Extracellular Matrix Enable Long-Range Stress Transmission between Cells Biophys. J. 2013 104 1410 1418
82. S. Münster L. M. Jawerth B. A. Leslie J. I. Weitz B. Fabry D. A. Weitz Strain history dependence of the nonlinear stress response of fibrin and collagen networks Proc. Natl. Acad. Sci. U. S. A. 2013 110 12197 12202
83. O. V. Kim R. I. Litvinov J. W. Weisel M. S. Alber Structural basis for the nonlinear mechanics of fibrin networks under compression Biomaterials 2014 35 6739 6749
84. A. Krammer H. Lu B. Isralewitz K. Schulten V. Vogel Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch Proc. Natl. Acad. Sci. U. S. A. 1999 96 1351 1356
85. Y. Mao J. E. Schwarzbauer Fibronectin fibrillogenesis, a cell-mediated matrix assembly process Matrix Biol. 2005 24 389 399
86. V. Vogel M. P. Sheetz Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways Curr. Opin. Cell Biol. 2009 21 38 46
87. R. O. Hynes The Extracellular Matrix: Not Just Pretty Fibrils Science 2009 326 1216 1219
88. C. A. Lemmon C. S. Chen L. H. Romer Cell Traction Forces Direct Fibronectin Matrix Assembly Biophys. J. 2009 96 729 738
89. S. P. Carey C. M. Kraning-Rush R. M. Williams C. A. Reinhart-King Biophysical control of invasive tumor cell behavior by extracellular matrix microarchitecture Biomaterials 2012 33 4157 4165
90. K. Wolf P. Friedl Mapping proteolytic cancer cell-extracellular matrix interfaces Clin. Exp. Metastasis 2009 26 289 298
91. D. Mitrossilis J. Fouchard A. Guiroy N. Desprat N. Rodriguez B. Fabry A. Asnacios Single-cell response to stiffness exhibits muscle-like behavior Proc. Natl. Acad. Sci. U. S. A. 2009 106 18243 18248
92. M. Mak D. Erickson Mechanical decision trees for investigating and modulating single-cell cancer invasion dynamics Lab Chip 2014 14 964 971
93. P. P. Provenzano D. R. Inman K. W. Eliceiri S. M. Trier P. J. Keely Contact Guidance Mediated Three-Dimensional Cell Migration is Regulated by Rho/ROCK-Dependent Matrix Reorganization Biophys. J. 2008 95 5374 5384
94. K. Wolf P. Friedl Extracellular matrix determinants of proteolytic and non-proteolytic cell migration Trends Cell Biol. 2011 21 736 744
95. P. Honarmandi H. Lee M. J. Lang R. D. Kamm A microfluidic system with optical laser tweezers to study mechanotransduction and focal adhesion recruitment Lab Chip 2011 11 684 694
96. W. J. Polacheck A. E. German A. Mammoto D. E. Ingber R. D. Kamm Mechanotransduction of fluid stresses governs 3D cell migration Proc. Natl. Acad. Sci. U. S. A. 2014 111 2447 2452
97. M. J. Dalby S. J. Yarwood M. O. Riehle H. J. H. Johnstone S. Affrossman A. S. G. Curtis Increasing Fibroblast Response to Materials Using Nanotopography: Morphological and Genetic Measurements of Cell Response to 13-nm-High Polymer Demixed Islands Exp. Cell Res. 2002 276 1 9
98. E. K. F. Yim E. M. Darling K. Kulangara F. Guilak K. W. Leong Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells Biomaterials 2010 31 1299 1306
99. C. J. Bettinger R. Langer J. T. Borenstein Engineering Substrate Topography at the Micro- and Nanoscale to Control Cell Function Angew. Chem., Int. Ed. 2009 48 5406 5415
100. M. Mak C. A. Reinhart-King D. Erickson Microfabricated Physical Spatial Gradients for Investigating Cell Migration and Invasion Dynamics PLoS One 2011 6 e20825
101. C. S. Chen M. Mrksich S. Huang G. M. Whitesides D. E. Ingber Geometric Control of Cell Life and Death Science 1997 276 1425 1428
102. S. I. Fraley Y. Feng R. Krishnamurthy D.-H. Kim A. Celedon G. D. Longmore D. Wirtz A distinctive role for focal adhesion proteins in three-dimensional cell motility Nat. Cell Biol. 2010 12 598 604
103. M. Mak R. D. Kamm M. H. Zaman Impact of Dimensionality and Network Disruption on Microrheology of Cancer Cells in 3D Environments PLoS Comput. Biol. 2014 10 e1003959
104. M. Mak C. A. Reinhart-King D. Erickson Elucidating mechanical transition effects of invading cancer cells with a subnucleus-scaled microfluidic serial dimensional modulation device Lab Chip 2013 13 340 348
105. P.-H. Wu A. Giri S. X. Sun D. Wirtz Three-dimensional cell migration does not follow a random walk Proc. Natl. Acad. Sci. U. S. A. 2014 111 3949 3954
106. R. J. Petrie H. Koo K. M. Yamada Generation of compartmentalized pressure by a nuclear piston governs cell motility in a 3D matrix Science 2014 345 1062 1065
107. Q. Shi R. P. Ghosh H. Engelke C. H. Rycroft L. Cassereau J. A. Sethian V. M. Weaver J. T. Liphardt Rapid disorganization of mechanically interacting systems of mammary acini Proc. Natl. Acad. Sci. U. S. A. 2014 111 658 663
108. C. Borau W. Polacheck R. Kamm J. Garcia-Aznar Probabilistic Voxel-Fe model for single cell motility in 3D In Silico Cell and Tissue Science 2014 1 2
109. A. Saez A. Buguin P. Silberzan B. Ladoux Is the Mechanical Activity of Epithelial Cells Controlled by Deformations or Forces? Biophys. J. 2005 89 L52 L54
110. M.-C. Kim D. M. Neal R. D. Kamm H. H. Asada Dynamic Modeling of Cell Migration and Spreading Behaviors on Fibronectin Coated Planar Substrates and Micropatterned Geometries PLoS Comput. Biol. 2013 9 e1002926
111. S. P. Palecek J. C. Loftus M. H. Ginsberg D. A. Lauffenburger A. F. Horwitz Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness Nature 1997 385 537 540
112. Q. Tseng I. Wang E. Duchemin-Pelletier A. Azioune N. Carpi J. Gao O. Filhol M. Piel M. Thery M. Balland A new micropatterning method of soft substrates reveals that different tumorigenic signals can promote or reduce cell contraction levels Lab Chip 2011 11 2231 2240
113. D. Irmia M. Toner Spontaneous migration of cancer cells under conditions of mechanical confinement Integr. Biol. 2009 1 506 512
114. M.-C. Kim C. Kim L. Wood D. Neal R. D. Kamm H. H. Asada Integrating focal adhesion dynamics, cytoskeleton remodeling, and actin motor activity for predicting cell migration on 3D curved surfaces of the extracellular matrix Integr. Biol. 2012 4 1386 1397
115. D. E. Discher P. Janmey Y.-l. Wang Tissue Cells Feel and Respond to the Stiffness of Their Substrate Science 2005 310 1139 1143
116. A. J. Engler S. Sen H. L. Sweeney D. E. Discher Matrix Elasticity Directs Stem Cell Lineage Specification Cell 2006 126 677 689
117. J. Swift I. L. Ivanovska A. Buxboim T. Harada P. C. D. P. Dingal J. Pinter J. D. Pajerowski K. R. Spinler J.-W. Shin M. Tewari F. Rehfeldt D. W. Speicher D. E. Discher Nuclear Lamin-A Scales with Tissue Stiffness and Enhances Matrix-Directed Differentiation Science 2013 341 1240104
118. T. Mammoto A. Mammoto D. E. Ingber Mechanobiology and Developmental Control Annu. Rev. Cell Dev. Biol. 2013 29 27 61
119. A. Zemel F. Rehfeldt A. E. X. Brown D. E. Discher S. A. Safran Optimal matrix rigidity for stress-fibre polarization in stem cells Nat. Phys. 2010 6 468 473
120. N. Chen J. A. Glazier J. A. Izaguirre M. S. Alber A parallel implementation of the Cellular Potts Model for simulation of cell-based morphogenesis Comput. Phys. Commun. 2007 176 670 681
121. T. Vicsek A. Zafeiris Collective motion Phys. Rep. 2012 517 71 140
122. A. J. Kabla Collective cell migration: leadership, invasion and segregation J. R. Soc., Interface 2012 9 3268 3278
123. F. Frascoli B. D. Hughes M. H. Zaman K. A. Landman A Computational Model for Collective Cellular Motion in Three Dimensions: General Framework and Case Study for Cell Pair Dynamics PLoS One 2013 8 e59249
124. S. Vedel S. Tay D. M. Johnston H. Bruus S. R. Quake Migration of cells in a social context Proc. Natl. Acad. Sci. U. S. A. 2013 110 129 134
125. E. Boghaert J. P. Gleghorn K. Lee N. Gjorevski D. C. Radisky C. M. Nelson Host epithelial geometry regulates breast cancer cell invasiveness Proc. Natl. Acad. Sci. U. S. A. 2012 109 19632 19637
126. D. T. Tambe C. Corey Hardin T. E. Angelini K. Rajendran C. Y. Park X. Serra-Picamal E. H. Zhou M. H. Zaman J. P. Butler D. A. Weitz J. J. Fredberg X. Trepat Collective cell guidance by cooperative intercellular forces Nat. Mater. 2011 10 469 475
127. M. Reffay M. C. Parrini O. Cochet-Escartin B. Ladoux A. Buguin S. Coscoy F. Amblard J. Camonis P. Silberzan Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells Nat. Cell Biol. 2014 16 217 223
128. O. Campas T. Mammoto S. Hasso R. A. Sperling D. O'Connell A. G. Bischof R. Maas D. A. Weitz L. Mahadevan D. E. Ingber Quantifying cell-generated mechanical forces within living embryonic tissues Nat. Methods 2014 11 183 189
129. D. E. Cameron C. J. Bashor J. J. Collins A brief history of synthetic biology Nat. Rev. Microbiol. 2014 12 381 390
130. P. E. M. Purnick R. Weiss The second wave of synthetic biology: from modules to systems Nat. Rev. Mol. Cell Biol. 2009 10 410 422
131. R. J. Ellis Macromolecular crowding: an important but neglected aspect of the intracellular environment Curr. Opin. Struct. Biol. 2001 11 114 119
132. M. Guo A. J. Ehrlicher M. H. Jensen M. Renz J. R. Moore R. D. Goldman J. Lippincott-Schwartz F. C. Mackintosh D. A. Weitz Probing the Stochastic, Motor-Driven Properties of the Cytoplasm Using Force Spectrum Microscopy Cell 2014 158 822 832
133. A. W. C. Lau B. D. Hoffman A. Davies J. C. Crocker T. C. Lubensky Microrheology, Stress Fluctuations, and Active Behavior of Living Cells Phys. Rev. Lett. 2003 91 198101
134. C. Wilhelm Out-of-Equilibrium Microrheology inside Living Cells Phys. Rev. Lett. 2008 101 028101
135. K. V. Iyer S. Pulford A. Mogilner G. V. Shivashankar Mechanical Activation of Cells Induces Chromatin Remodeling Preceding MKL Nuclear Transport Biophys. J. 2012 103 1416 1428
136. C. Guilluy L. D. Osborne L. Van Landeghem L. Sharek R. Superfine R. Garcia-Mata K. Burridge Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus Nat. Cell Biol. 2014 16 376 381
137. B. Wunderlich D. Nettels S. Benke J. Clark S. Weidner H. Hofmann S. H. Pfeil B. Schuler Microfluidic mixer designed for performing single-molecule kinetics with confocal detection on timescales from milliseconds to minutes Nat. Protoc. 2013 8 1459 1474
138. M. Soltani J. Lin R. A. Forties J. T. Inman S. N. Saraf R. M. Fulbright M. Lipson M. D. Wang Nanophotonic trapping for precise manipulation of biomolecular arrays Nat. Nanotechnol. 2014 9 448 452
139. J. Kang K. M. Puskar A. J. Ehrlicher P. R. LeDuc R. S. Schwartz Structurally Governed Cell Mechanotransduction through Multiscale Modeling Sci. Rep. 2015 5 10.1038/srep08622