Measurement techniques for cellular biomechanics in vitro

Experimental Biology and Medicine

Volumn 233, Issue 7, 2008, Pages 792-809

  Addae Mensah, Kweku A ^a,b   Wikswo, John P ^a,b,c  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atomic force microscopy (AFM); Carbon fibers; Force sensors; Magnetic tweezers; Magnetic twisting cytometry; Microcantilever arrays; Micropipette aspiration; Optical tweezers; Polydimethylsiloxane (PDMS); Traction force microscopy

Indexed keywords

ACTIN; CARBON FIBER; QUANTUM DOT;

ANALYTIC METHOD; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CELL ADHESION; CELL STRAIN; CHICKEN; CYTOMETRY; DEVICE; ERYTHROCYTE MEMBRANE; FEEDBACK SYSTEM; FIBROBLAST; HEART MUSCLE CELL; HUMAN; IN VITRO STUDY; MAGNETISM; MECHANICAL TORSION; MECHANOTRANSDUCTION; NONHUMAN; RIGIDITY; SHEAR FLOW; SHEAR STRESS; SHORT SURVEY; SMOOTH MUSCLE FIBER; SURFACE TENSION; THROMBOCYTE; VISCOELASTICITY; YOUNG MODULUS; ANIMAL; CELL; CELL FUNCTION; CYTOLOGY; INSTRUMENTATION; MECHANICAL STRESS; METHODOLOGY; REVIEW;

ANIMALS; BIOMECHANICS; CELL PHYSIOLOGY; CELLS; CYTOLOGICAL TECHNIQUES; HUMANS; MICROSCOPY, ATOMIC FORCE; STRESS, MECHANICAL;

EID: 47749110611     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.3181/0710-MR-278     Document Type: Short Survey

References (81)

1. Stopak D, Wessells NK, Harris AK. Morphogenetic rearrangement of injected collagen in developing chicken limb buds. Proc Natl Acad Sci 82:2804-2808, 1985.
2. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139-1143, 2005.
3. Kung C. A possible unifying principle for mechanosensation. Nature 436:647-654, 2005.
4. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. FASEB J 20:811-827, 2006.
5. Ali MH, Schumacker PT. Endothelial responses to mechanical stress: where is the mechanosensor? Crit Care Med 30:S198-S206, 2002.
6. Lehoux S, Tedgui A. Cellular mechanics and gene expression in blood vessels. J Biomech 36:631-643, 2003.
7. Grodzinsky AJ, Levenston ME, Jin M, Frank EH. Cartilage tissue remodeling in response to mechanical forces. Annu Rev of Biomed Eng 2:691-713, 2000.
8. Herberhold C, Faber S, Stammberger T, Steinlechner M, Putz R, Englmeier KH, Reiser M, Eckstein F. In situ measurement of articular cartilage deformation in intact femoropatellar joints under static loading. J Biomech 32:1287-1295, 1999.
9. van Netten SM, Kros CJ. Gating energies and forces of the mammalian hair cell transducer channel and related hair bundle mechanics. Proc R Soc Lond B Biol Sci 267:1915-1923, 2000.
10. Liao ZJ, Feng S, Popel AS, Brownell WE, Spector AA. Outer hair cell active force generation in the cochlear environment. J Acoust Soc Am 122:2215-2225, 2007.
11. Maffulli N, Wong J. Rupture of the Achilles and patellar tendons. Clin Sports Med 22:761-776, 2003.
12. Yin SH, Zhang XQ, Zhan C, Wu JT, Xu JC, Cheung J. Measuring single cardiac myocyte contractile force via moving a magnetic bead. Biophys J 88:1489-1495, 2005.
13. Smith DH, Wolf JA, Meaney DF. A new strategy to produce sustained growth of central nervous system axons: continuous mechanical tension. Tissue Eng 7:131-139, 2001.
14. Shore SA, Moore PE. Regulation of [beta]-adrenergic responses in airway smooth muscle. Respir Physiol Neurobiol 137:179-195, 2003.
15. Radmacher M, Fritz M, Kacher CM, Cleveland JP, Hansma PK. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys J 70:556-567, 1996.
16. Radmacher M, Tillmann RW, Gaub HE. Imaging viscoelasticity by force modulation with the atomic force microscope. Biophys J 64:735-742, 1993.
17. Weisenhorn AL, Khorsandi M, Kasas S, Gotzos V, Butt H-J. Deformation and height anomaly of soft surfaces studied with an AFM. Nanotechnology 4:106-113, 1993.
18. Hoh JH, Schoenenberger CA. Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy. J Cell Sci 107:1105-1114, 1994.
19. Mathur AB, Collinsworth AM, Reichert WM, Kraus WE, Truskey GA. Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J Biomech 34:1545-1553, 2001.
20. Crick FHC, Hughes AFW. The physical properties of cytoplasm: a study by means of the magnetic particle method Part I. Experimental. Exp Cell Res 1:37-80, 1950.
21. Lele TP, Sero JE, Matthews BD, Kumar S, Xia S, Polte T, Overby D, Wang N, Ingber DE. Methods in cell biology. In: Wang Y-L, Discher DE, Eds. Cell Mechanics. New York: Academic Press, pp443-472, 2007.
22. Ziemann F, Radler J, Sackmann E. Local measurements of viscoelastic moduli of entangled actin networks using an oscillating magnetic bead micro-rheometer. Biophys J 66:2210-2216, 1994.
23. Bausch AR, Moller W, Sackmann E. Measurement of local viscoelasticity and forces in living cells by magnetic tweezers. Biophys J 76:573-579, 1999.
24. Wang N, Butler JP, Ingber DE. Mechanotransduction across the cell-surface and through the cytoskeleton. Science 260:1124-1127, 1993.
25. Chen J, Fabry B, Schiffrin EL, Wang N. Twisting integrin receptors increases endothelin-1 gene expression in endothelial cells. Am J Physiol Cell Physiol 280:C1475-C1484, 2001.
26. Chien S, Sung KL, Skalak R, Usami S, Tozeren A. Theoretical and experimental studies on viscoelastic properties of erythrocyte membrane. Biophys J 24:463-487, 1978.
27. Schmid-Schonbein GW, Sung KL, Tozeren H, Skalak R, Chien S. Passive mechanical properties of human leukocytes. Biophys J 36:243-256, 1981.
28. Hiramoto Y. Methods in cell biology. In: Schroeder TE, Ed. Echinoderm Gametes and Embryos. New York: Academic Press, Inc., pp435-442, 1986.
29. Jones WR, Ping Ting-Beall H, Lee GM, Kelley SS, Hochmuth RM, Guilak F. Alterations in the Young's modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. J Biomech 32:119-127, 1999.
30. Alexopoulos LG, Haider MA, Vail TP, Guilak F. Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. J Biomech Eng 125:323-333, 2003.
31. Chu YS, Thomas WA, Eder O, Pincet F, Perez E, Thiery JP, Dufour S. Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J Cell Biol 167:1183-1194, 2004.
32. Henon S, Lenormand G, Richert A, Gallet F. A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys J 76:1145-1151, 1999.
33. Dao M, Lim CT, Suresh S. Mechanics of the human red blood cell deformed by optical tweezers. J Mech Phys Solids 51:2259-2280, 2003 and J Mech Phys Solids 53:493-494. 2005.
34. Grayson ACR, Shawgo RS, Johnson AM, Flynn NT, Yawen LI, Cima MJ, Langer R. A BioMEMS review: MEMS technology for physiologically integrated devices. Proc IEEE 92:6-21, 2004.
35. Xia Y, Whitesides GM. Soft lithography. Annu Rev Mater Sci 28:153-184, 1998.
36. McDonald JC, Duffy DC, Anderson JR, Chiu DT, Wu HK, Schueller OJA, Whitesides GM. Fabrication of microfluidic systems in poly (dimethylsiloxane). Electrophoresis 21:27-1-0, 2000.
37. Yang S, Saif T. Micromachined force sensors for the study of cell mechanics. Rev Sci Instrum 76:044301-044308, 2005.
38. Serrell DB, Oreskovic TL, Slifka AJ, Mahajan RL, Finch DS. A uniaxial bioMEMS device for quantitative force-displacement measurements. Biomed Microdevices 9:267-275, 2007.
39. Hochmuth RM, Mohandas N, Blackshear PL. Measurement of the elastic modulus for red cell membrane using a fluid mechanical technique. Biophys J 13:747-762, 1973.
40. 2+-independent signaling mechanism. J Appl Physiol 93:1907-1917, 2002.
41. Ainslie KM, Garanich JS, Dull RO, Tarbell JM. Vascular smooth muscle cell glycocalyx influences shear stress-mediated contractile response. J Appl Physiol 98:242-249, 2005.
42. Frangos JA, Eskin SG, McIntire LV, Ives CL. Flow effects on prostacyclin production by cultured human endothelial cells. Science 227:1477-1479, 1985.
43. Cao J, Usami S, Dong C. Development of a side-view chamber for studying cell-surface adhesion under flow conditions. Ann of Biomed Eng 25:573-580, 1997.
44. Dong C, Cao J, Struble EJ, Lipowsky HW. Mechanics of leukocyte deformation and adhesion to endothelium in shear flow. Ann Biomed Eng 27:298-312, 1999.
45. Leyton-Mange J, Yang S, Hoskins MH, Kunz RF, Zahn JD, Dong C. Design of a side-view particle imaging velocimetry flow system for cell-substrate adhesion studies. J Biomech Eng-Trans ASME 128:271-278, 2006.
46. Wang JHC, Goldschmidt-Clermont P, Yin FCP. Contractility affects stress fiber remodeling and reorientation of endothelial cells subjected to cyclic mechanical stretching. Ann Biomed Eng 28:1165-1171, 2000.
47. Zhuang JP, Yamada KA, Saffitz JE, Kleber AG. Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ Res 87: 316-322, 2000.
48. Yasuda Si, Sugiura S, Kobayakawa N, Fujita H, Yamashita H, Katoh K, Saeki Y, Kaneko H, Suda Y, Nagai R, Sugi H. A novel method to study contraction characteristics of a single cardiac myocyte using carbon fibers. Am J Physiol Heart Circ Physiol 281:H1442-H1446, 2001.
49. Nishimura S, Yasuda Si, Katoh M, Yamada KP, Yamashita H, Saeki Y, Sunagawa K, Nagai R, Hisada T, Sugiura S. Single cell mechanics of rat cardiomyocytes under isometric, unloaded, and physiologically loaded conditions. Am J Physiol Heart Circ Physiol 287:H196-H202, 2004.
50. Iribe G, Helmes M, Kohl P. Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load. Am J Physiol Heart Circ Physiol 292:H1487-H1497, 2007.
51. Harris AK, Wild P, Stopak D. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208:177-179, 1980.
52. Danowski BA. Fibroblast contractility and actin organization are stimulated by microtubule inhibitors. J Cell Sci 93:255-266, 1989.
53. Lee J, Leonard M, Oliver T, Ishihara A, Jacobson K. Traction forces generated by locomoting keratocytes. J Cell Biol 127:1957-1964, 1994.
54. Pelham RJ Jr, Wang YL. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci 94:13661-13665, 1997.
55. Dembo M, Wang YL. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J 76:2307-2316, 1999.
56. Munevar S, Wang YL, Dembo M. Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophys J 80: 1744-1757, 2001.
57. Butler JP, Tolic-Norrelykke IM, Fabry B, Fredberg JJ. Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol Cell Physiol 282:C595-C605, 2002.
58. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, Mahalu D, Safran S, Bershadsky A, Addadi L, Geiger B. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nature Cell Biol 3:466-472, 2001.
59. Galbraith CG, Sheetz MP. A micromachined device provides a new bend on fibroblast tractionaforces. Proc Natl Acad Sci 94:9114-9118, 1997.
60. Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci 100:1484-1489, 2003.
61. Roure OD, Dequidt C, Richert A, Austin RH, Buguin A, Chavrier P, Silberzan P, Ladoux B. Microfabricated arrays of elastomeric posts to study cellular mechanics. Proc SPIE 5345:26-34, 2004.
62. du Roure O, Saez A, Buguin A, Austin RH, Chavrier P, Silberzan P, Ladoux B. Force mapping in epithelial cell migration. Proc Natl Acad Sci 102:2390-2395, 2005.
63. Petronis S, Gold J, Kasemo B. Microfabricated force-sensitive elastic substrates for investigation of mechanical cell-substrate interactions. J Micromech Microeng 13:900-913, 2003.
64. Addae-Mensah KA, Kassebaum NJ, Bowers MJ II, Reiserer RS, Rosenthal SJ, Moore PE, Wikswo JP. A flexible, quantum dot-labeled cantilever post array for studying cellular microforces. Sensor Actuat A-Phys 136:385-397, 2007.
65. McKnight TE, Melechko AV, Griffin GD, Guillorn MA, Merkulov VI, Serna F, Hensley DK, Doktycz MJ, Lowndes DH, Simpson ML. Intracellular integration of synthetic nanostructures with viable cells for controlled biochemical manipulation. Nanotechnology 14:551-556, 2003.
66. McKnight TE, Melechko AV, Hensley DK, Mann DGJ, Griffin GD, Simpson ML. Tracking gene expression after DNA delivery using spatially indexed nanofiber arrays. Nano Lett 4:1213-1219, 2004.
67. Fletcher BL, McKnight TE, Melechko AV, Simpson ML, Doktycz MJ. Biochemical functionalization of vertically aligned carbon nanofibres. Nanotech 17:2032-2039, 2006.
68. Kim W, Ng JK, Kunitake ME, Conklin BR, Yang P. Interfacing silicon nanowires with mammalian cells. J Am Chem Soc 129:7228-7229, 2007.
69. Wang N, Tolic-Norrelykke IM, Chen J, Mijailovich SM, Butler JP, Fredberg JJ, Stamenovic D. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am J Physiol Cell Physiol 282:C606-C616, 2002.
70. Addae-Mensah KA, Reiserer RS, Wikswo JP. Poly(vinyl alcohol) as a structure release layer for the microfabrication of polymer composite structures. J Micromech Microeng 17:N41-N46, 2007.
71. Sniadecki NJ, Anguelouch A, Yang MT, Lamb CM, Liu Z, Kirschner SB, Liu Y, Reich DH, Chen CS. Magnetic microposts as an approach to apply forces to living cells. Proc Natl Acad Sci 104:14553-14558, 2007.
72. Waggoner PS, Craighead HG. Micro- and nanomechanical sensors for environmental, chemical, and biological detection. Lab Chip 7:1238-1255, 2007.
73. Kumar S, Maxwell IZ, Heisterkamp A, Polte TR, Lele TP, Salanga M, Mazur E, Ingber DE. Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J 90:3762-3773, 2006.
74. Hutson MS, Tokutake Y, Chang MS, Bloor JW, Venakides S, Kiehart DP, Edwards GS. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300:145-149, 2003.
75. Peralta XG, Toyama Y, Hutson MS, Montague R, Venakides S, Kiehart DP, Edwards GS. Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys J 92: 2583-2596, 2007.
76. Finer JT, Simmons RM, Spudich JA. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368:113-119, 1994.
77. Bustamante C, Bryant Z, Smith SB. Ten years of tension: single-molecule DNA mechanics. Nature 421:423-427, 2003.
78. Wuite GJL, Smith SB, Young M, Keller D, Bustamante C. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404:103-106, 2000.
79. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM. Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241-254, 2005.
80. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 126:677-689, 2006.
81. Furukawa KS, Ushida T, Nagase T, Nakamigawa H, Noguchi T, Tamaki T, Tanaka J, Tateishi T. Quantitative analysis of cell detachment by shear stress. Mater Sci Eng C17:55-58, 2001.