The biomechanics toolbox: Experimental approaches for living cells and biomolecules

Acta Materialia

Volumn 51, Issue 19, 2003, Pages 5881-5905

  Van Vliet, K J ^a,b   Bao, G ^c   Suresh, S ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c Emory University   (United States)

Author keywords

Biomechanics; Elastic behavior; Macromolecular materials; Stress rupture

Indexed keywords

BIOLOGICAL MATERIALS; CELLS; DISEASES; ELASTICITY; HEALTH CARE; MACROMOLECULES; STRESS ANALYSIS; TISSUE;

BIOMOLECULES;

BIOMECHANICS;

EID: 0142029493     PISSN: 13596454     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actamat.2003.09.001     Document Type: Article

References (106)

1. Feeback DL, Clarke MSF. Improved unidirectional cell-stretching device. In: Book Improved unidirectional cell-stretching device. http://www.nasatech.com/Briefs/Aug00/MSC22834.html ; 2000.
2. Pelham R.J., Wang Y.-L. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proceedings of the National Academy of Science USA. 94:1997;13661-13665.
3. Beningo K.A., Wang Y.-L. Flexible substrata for the detection of cellular traction forces. Trends in Cell Biology. 12:2002;79-84.
4. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., Chen C.S. Cells lying on a bed of microneedles: An approach to isolate mechanical force. Proceedings of the National Academy of Science. 100:2003;1484-1489.
5. Fabry B., Butler J.P., Navajas D., Tschumperlin D.J., Laporte J.D., Maksym G.N., Fredberg J.J. Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 4 Hz. J Appl Physiol. 89:2000.
6. Puig-de-Morales M., Grabulosa M., Alcaraz J., Mullol J., Maksym G.N., Fredberg J.J., Navajas D. Measurement of cell microrheology by magnetic twisting cytometry with frequency domain demodulation. Journal of Applied Physiology. 91:2001;1152-1159.
7. Maksym G.N., Fabry B., Butler J.P., Navajas D., Tschumperlin D.J., Laporte J.D., Fredberg J.J. Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. Journal of Applied Physiology. 89:2000;1619-1632.
8. Athanasiou K.A., Thoma B.S., Lanctot D.R., Shin D., Agrawal C.M., LeBaron R.G. Development of the cytodetachment technique to quantify mechanical adhesiveness of the single cell. Biomaterials. 20:1999;2405-2415.
9. Yeung A., Evans E. Cortical shell-liquid core model for passive flow of liquid-like spherical cells into micropipets. Biophysical Journal. 56:1989;139-149.
10. Evans E., Yeung A. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophysical Journal. 56:1989;151-160.
11. Ananthakrishnan R., Moon T.J., Cunningham C.C., Guck K.J.J. Optical deformability of soft biological dielectrics. Physical Review Letters. 84:2000;5451-5454.
12. Wu H.W., Kuhn T., Moy V.T. Mechanical properties of l929 cells measured by atomic force microscopy: Effects of anticytoskeletal drugs and membrane crosslinking. Scanning. 20:1998;389-397.
13. Radmacher M. Measuring the elastic properties of living cells by the atomic force microscope. Atomic Force Microscopy in Cell Biology. 68:2002;67-90.
14. Czajkowsky D.M., Shao Z.F. Supported lipid bilayers as effective substrates for atomic force microscopy. Atomic Force Microscopy in Cell Biology. 68:2002;231-241.
15. Goldmann W.H. Mechanical manipulation of animal cells: cell indentation. Biotechnology Letters. 22:2000;431-435.
16. Rotsch C., Braet F., Wisse E., Radmacher M. AFM imaging and elasticity measurements on living rat liver macrophages. Cell Biol Int. 21:1997;685-696.
17. Rotsch C., Radmacher M. Drug induced changes in cytoskeletal structure and mechanics in fibroblasts-An atomic force microscopy study. Biophysical Journal. 78:2000;520-535.
18. Benoit M. Cell adhesion measured by force spectroscopy on living cells. Atomic Force Microscopy in Cell Biology. 68:2002;91-114.
19. Chen A.L., Moy V.T. Single-molecule force measurements. Atomic Force Microscopy in Cell Biology. 68:2002;301-309.
20. Felder S., Elson E.L. Mechanics of fibroblast locomotion: Quantitative analysis of forces and motions at the leading lamellas of fibroblasts. Journal of Cell Biology. 111:1990;2513-2526.
21. Peterson N.O., McConnaughey W.B., Elson E.L. Dependence of locally measured cellular deformability on position in the cell, temperature and cytochalasin B. Proceedings of the National Academy of Sciences USA. 79:1982;5327-5331.
22. Sleep J., Wilson D., Simmons R., Gratzer W. Elasticity of the red cell membrane and its relation to hemolytic disorders: An optical tweezers study. Biophysical Journal. 77:1999;3085-3095.
23. Bausch A.R., Ziemann F., Boubitch A.A., Jacobson K., Sackmann E. Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead rheometry. Biophysical Journal. 75:1998;2038-2049.
24. Crick F.H.C., Hughes A.F.W. The physical properties of the cytoplasm. a study by the means of the magnetic particle method. Experimental Cell Research. 1:1965;37-80.
25. Bausch A.R., Moller W., Sackmann E. Measurement of local viscoelasticity and forces in living cells by magnetic tweezers. Biophysical Journal. 76:1999;573-579.
26. Alenghat F.J., Fabry B., Tsai K.Y., Goldmann W.H., Ingber D.E. Analysis of cell mechanics in single vinculin-deficient cells using a magnetic tweezer. Biochemical and Biophysical Research Communications. 277:2000;93-99.
27. Brown T.D. Techniques for mechanical stimulation of cells in vitro: A review. Journal of Biomechanics. 33:2000;3-14.
28. Pioletti D.P., Muller J., Rakotomanana L.R., Corbeil J., Wild E. Effect of micromechanical stimulations on osteoblasts: development of a device simulating the mechanical situation at the bone-implant interface. Journal of Biomechanics. 36:2003;131-135.
29. Lee A.A., Delhaas T., Waldman L.K., MacKenna D.A., Villarreal F.J., McCulloch A.D. An equibiaxial strain system for cultured cells. American Journal of Physiology-Cell Physiology. 40:1996;C1400-C1408.
30. Zhu C., Bao G., Wang N. Cell mechanics: Mechanical response, cell adhesion, and molecular deformation. Annual Review of Biomedical Engineering. 2:2000;189-226.
31. Jones D.B., Nolte H., Scholubbers G.E., Turner J., Veltel D. Biochemical signal transduction of mechanical strain in oseoblast-like cells. Biomaterials. 12:1991;101-110.
32. Dunn A, Moses MA, Van Vliet KJ. Effects of radial, cyclic strain on enzyme activity in endothelial cells 2003 (in preparation).
33. Wang H.C., Ip W., Boissy R., Grood E.S. Cell orientation response to cyclically deformed substrates: Experimental validation of a cell model. Journal of Biomechanics. 1995:1543;28.
34. Pfister B.J., Weihs T.P., Betenbaugh M., Bao G. An in vitro uniaxial stretch model for axonal injury. Ann Biomed Eng. 31:2003;589-598.
35. Cohen Y, Ramon O, Kopelman IJ, Mizrahi S. Journal of Polymer Science B 1992;30:1055-1067.
36. Lo C.-M., Wang H.-B., Dembo M., Wang Y.-L. Cell movement is guided by the rigidity of the substrates. Biophys J. 79:2000;144-152.
37. Lo C-M, Wang H-B, Dembo M, Wang YL. http://ylwang.umassmed.edu/video/guidance.htm, City 2000.
38. Wang N., Ostuni E., Whitesides G.M., Ingber D.E. Micropatterning tractional forces in living cells. Cell Motility and the Cytoskeleton. 52:2002;97-106.
39. Munevar S., Dembo M., Wang Y.-L. Traction force microscopy of normal and transformed fibroblasts. Biophys J. 80:2001;1744-1757.
40. Butler J.P., Wang N., Ingber D.E. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 260:1993;124-1127.
41. Fabry B., Maksym G.N., Hubmayr R.D., Butler J.P., Fredberg J.J. Implications of heterogeneous bead behavior on cell mechanical properties measured with magnetic twisting cytometry. Journal of Magnetism and Magnetic Materials. 194:1999;120-125.
42. Dike L.E., Chen C.S., Mrksich M., Tien J., Whitesides G.M., Ingber D.E. Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropattened substrates. In vitro Cell Dev Biol. 35:1999;441-448.
43. Parker K.K., Brock A.L., Brangwynne C., Mannix R.J., Wang N., Ostuni E., Geisse N.A., Adams J.C., Whitesides G.M., Ingber D.E. Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces. FASEB. 16:2002;1195-1204.
44. Singhvi R., Kumar A., Lopez G.P., Stephanopoulos G.N., Wang D.I.C., Whitesides G.M., Ingber D.E. Engineering cell shape and function. Science. 264:1994;696-699.
45. Xia Y., Whitesides G.M. Soft lithography. Ann Rev Mater Sci. 28:1998;153-184.
46. Hochmuth R.M. Micropipette aspiration of living cells. Journal of Biomechanics. 33:2000;15-22.
47. Shao J-Y. Measuring piconewton forces and its application in cellular and molecular biomechanics. Advances in Biomechanics 2001:47-51.
48. Hochmuth R.M., Ting-Beall H.B., Beaty B.B., Needham D., Tran-Son-Tay R. Viscosity of passive human neutrophils undergoing small deformations. Biophysical Journal. 64:1993;1596-1601.
49. Sato J., Levesque M.J., Nerem R.M. Micropipette aspiration of cultured bovine aortic endothelial cells exposed to shear stress. Arteriosclerosis. 7:1987;276-286.
50. Jones W.R., Ting-Beall H.P., Lee G.M., Kelley S.S., Hochmuth R.M., Guilak F. Alterations in the Young's modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. Journal of Biomechanics. 32:1999;119-127.
51. Secomb T.W. Red-blood-cell mechanics and capillary blood rheology. Cell Biophysics. 18:1991;231-251.
52. Secomb T.W., Hsu R. Red blood cell mechanics and functional capillary density. International Journal of Microcirculation-Clinical and Experimental. 15:1995;250-254.
53. Wu J.Z., Herzog W., Epstein M. Modelling of location- and time-dependent deformation of chondrocytes during cartilage loading. Journal of Biomechanics. 32:1999;563-572.
54. Wu J.Z., Herzog W. Finite element simulation of location- and time-dependent mechanical behavior of chondrocytes in unconfined compression tests. Annals of Biomedical Engineering. 28:2000;318-330.
55. Guilak F., Mow V.C. The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. Journal of Biomechanics. 33:2000;1663-1673.
56. Haider M.A., Guilak F. An axisymmetric boundary integral model for incompressible linear viscoelasticity: Application to the micropipette aspiration contact problem. Journal of Biomechanical Engineering-Transactions of the ASME. 122:2000;236-244.
57. Haider M.A., Guilak F. An axisymmetric boundary integral model for assessing elastic cell properties in the micropipette aspiration contact problem. Journal of Biomechanical Engineering-Transactions of the ASME. 124:2002;586-595.
58. Boey SK, Boal DH, Discher DE. Biophysical Journal 1998;75:1573-1583.
59. Discher DE, Boad DH, Boey SK. Biophysical Journal 1998;75:1584-1597.
60. Lim CT, Lee YS, Tan K, Dao M, Suresh S. National University of Singapore and Massachusetts Institute of Technology. National University of Singapore and Massachusetts Institute of Technology; 2003 (unpulbished results).
61. Ashkin A. Optical Letters 1986;11:288.
62. Ashkin A., Dziedzic J.M. Optical trapping and manipulation of viruses and bacteria. Science. 235:1987;1517-1520.
63. Smith S.B., Cui Y., Bustamante C. An optical-trap force transducer that operates by direct measurement of light momentum. Methods in Enzymology. 79:2002;144-152.
64. Williams M.C. Optical tweezers: Measuring piconewton forces. Schwille P. Single Molecule Techniques. 2002;Biophysics Textbook Online.
65. Gittes F, Schmidt C. In: L. Wilson, M. Sheetz, P. Matsudaira (Eds.), Laser Tweezers in Cell Biology. San Diego: Academic Press; 1998.
66. Chew KT, Lim CT, Sow CH, Dao M, Suresh S. Large deformation of human red blood cell by direct stretch using optical tweezers. 2003 (in preparation).
67. Dao M, Lim CT, Suresh S. Mechanics of the human red blood cell deformed by optical tweezers. J Mech Phys Solids 2003, (in press).
68. Henon S, Lenormand G, Richert A, Gallet F. Biophys J 1999;76:1145-1151.
69. Sleep J, Wilson D, Simmons R, Gratzer W. Biophys J 1999;77:3085-3095.
70. Lenormand G, Henon S, Richert A, Gallet F. Biophys J 2001;81:43-56.
71. Prentiss H. Unpublished discussion of four optical traps to manipulate cells. http://atomsun.harvard.edu/; 2003.
72. Curtis J.E., Koss B.A., Grier D.G. Dynamic holographic optical tweezers. Opt Comm. 207:2002;169-175.
73. Mehta A.D., Rief M., Spudich J.A., Smith D.A., Simmons R.M. Single-molecule biomechanics with optical methods. Science. 283:1999;1689-1695.
74. Svoboda K., Block S.M., Asbury C.L., Shaevitz J.W., Lang M.J. Force and velocity measured for single kinesin molecules. Cell. 77:1994;773-784.
75. Guck J., Chiang J.A., Kas J. The optical stretcher: A novel tool to characterize the cytoskeleton. Molecular Biology of the Cell. 9:1998;609.
76. Guck J., Ananthakrishnan R., Moon T.J., Cunningham C.C., Kas J. Optical deformability of soft biological dielectrics. Physical Review Letters. 84:2000;5451-5454.
77. Guck J., Ananthakrishnan R., Moon T.J., Cunningham C.C., Kas J. Optical deformability of cells. Biophysical Journal. 78:2000;2170Pos.
78. Guck J., Ananthakrishnan R., Mahmood H., Moon T.J., Cunningham C.C., Kas J. The optical stretcher: A novel laser tool to micromanipulate cells. Biophysical Journal. 81:2001;767-784.
79. Guck J., Ananthakrishnan R., Mahmood H., Moon T.J., Cunningham C.C., Hallworth R., Kas J. The optical stretcher-A novel laser tool to micromanipulate cells. Biophysical Journal. 80:2001;1138.
80. Guck J., Ananthakrishnan R., Cunningham C.C., Kas J. Stretching biological cells with light. Journal of Physics-Condensed Matter. 14:2002;4843-4856.
81. Kas J., Guck J., Chiang J.A. The optical stretcher - A novel tool to manipulate cells. Biophysical Journal. 76:1999;A276-A276.
82. Moore S.A., Guck J., Ananthakrishnan R., Cunningham C.C., Kas J.A. The reverse progression of cancer in HL-60 cells as monitored by optical deformability. Biophysical Journal. 2002:1683;82.
83. Smith S.B., Finzi L., Bustamante C. Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science. 258:1992;1122-1126.
84. Strick T.R., Allemand J.F., Bensimon D., Bensimon A., Croquette V. The elasticity of a single supercoiled DNA molecule. Science. 271:1996;1835-1837.
85. Gosse C., Croquette V. Magnetic tweezers: Micromanipulation and force measurement at the molecular level. Biophysical Journal. 82:2002;3314-3329.
86. Hwang W.C., Waugh R.E. Energy of dissociation of lipid bilayer from the membrane skeleton of red blood cells. Biophysical Journal. 72:1997;2669-2678.
87. Ishijima A., Doi T., Sakurada K., Yanagida T. Sub-piconewton force fluctuations of actomyosin in vitro. Nature. 352:1991;301-306.
88. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Physical Review Letters. 56:1986;930-934.
89. Barbee K.A. Changes in surface topography in endothelial monolayers with time at confluence: Influence on subcellular shear stress distribution due to flow. Biochemistry and Cell Biology-Biochimie Et Biologie Cellulaire. 73:1995;501-505.
90. Charras G., Lehenkari P., Horton M. Biotechnological applications of atomic force microscopy. Atomic Force Microscopy in Cell Biology. 68:2002;171-191.
91. Kumar S., Hoh J.H. Probing the machinery of intracellular trafficking with the atomic force microscope. Traffic. 2:2001;746-756.
92. Lesniewska E., Milhiet P.E., Giocondi M.C., Le Grimellec C. Atomic force microscope imaging of cells and membranes. Atomic Force Microscopy in Cell Biology. 68:2002;51-65.
93. Domke J., Dannohl S., Parak W.J., Muller O., Aicher W.K., Radmacher M. Substrate dependent differencs in morphology and elasticity of living osteoblasts investigated by atomic force microscopy. Colloid Surfaces B. 19:2000;367-373.
94. Hinterdorfer P. Molecular recognition studies using the atomic force microscope. Atomic Force Microscopy in Cell Biology. 68:2002;115-139.
95. Ng L, Grodzinsky A, Plaas A, Sandy J, Ortiz C. J Struct Bio (in press).
96. Seog J, Dean D, Plaas A, Wong-Palms S, Grodzinsky A, Ortiz C. Macromolecules 2002;35:5601-5615.
97. Sneddon I.N. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. International Journal of Engineering Science. 3:1965;47-57.
98. Willemsen O.H., Snel M.M., Cambi A., Greve J., De Grooth B.G., Figdor C.G. Biomolecular interactions measured by atomic force microscopy. Biophys J. 79:2000;3267-3281.
99. Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C. Direct observation of catch bonds. Nature 2003.
100. Evans E. Probing the relation between force, lifetime and chemistry in single molecular bonds. Annual Review of Biophysics and Biomolecular Structure. 30:2001;105-128.
101. Merkel R., Nassoy P., Leung A., Ritchie K., Evans E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:1999;50-53.
102. G. Bao, S. Suresh, 2003, Cell and molecular mechanics of biological materials. MIT Nature Materials, 2003;2:715-25.
103. Glenister FK, Coppel RL, Cowman AF, Mohandas N, Cooke BM. Blood 2002;99:1060-1063.
104. Cooke BM, Mohandas N, Coppel RL. Adv Parasitology 2001;50:1-86.
105. Freyman T.M., Yannas I.V., Yokoo R., Gibson L.J. Fibroblast contraction of a collagen-GAG matrix. Biomaterials. 22:2001;2883-2891.
106. Guck J. Private communication with K.J. Van Vliet, 2003.