Microtissue Elasticity: Measurements by Atomic Force Microscopy and Its Influence on Cell Differentiation

Methods in Cell Biology

Volumn 83, Issue , 2007, Pages 521-545

  Engler, Adam J ^a   Rehfeldt, Florian ^a   Sen, Shamik ^a   Discher, Dennis E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ATOMIC FORCE MICROSCOPY; CAROTID ARTERY; CELL DIFFERENTIATION; CYTOLOGY; ELASTICITY; EXTRACELLULAR MATRIX; FEMALE; HYDROGEL; METABOLISM; METHODOLOGY; MOUSE; REVIEW; SKELETAL MUSCLE; SWINE;

ANIMALS; CAROTID ARTERIES; CELL DIFFERENTIATION; ELASTICITY; EXTRACELLULAR MATRIX; FEMALE; HYDROGELS; MICE; MICROSCOPY, ATOMIC FORCE; MUSCLE, SKELETAL; SWINE;

EID: 34347224040     PISSN: 0091679X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0091-679X(07)83022-6     Document Type: Review

References (59)

1. Alenghat F.J., and Ingber D.E. Mechanotransduction: All signals point to cytoskeleton, matrix, and integrins. Sci. STKE 2002 (2002) PE6
2. Barton-Davis E.R., Shoturma D.I., Musaro A., Rosenthal N., and Sweeney H.L. Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function. Proc. Natl. Acad. Sci. USA 95 (1998) 15603-15607
3. Beningo K.A., Lo C.M., and Wang Y.L. Flexible polyacrylamide substrata for the analysis of mechanical interactions at cell-substratum adhesions. Methods Cell Biol. 69 (2002) 325-339
4. Bershadsky A., Kozlov M., and Geiger B. Adhesion-mediated mechanosensitivity: A time to experiment, and a time to theorize. Curr. Opin. Cell Biol. 18 (2006) 472-481
5. Binnig G., Quate C.F., and Gerber C. Atomic force microscope. Phys. Rev. Lett. 56 (1986) 930-933
6. Buckley I.K., and Porter K.R. Cytoplasmic fibrils in living cultured cells. A light and electron microscope study. Protoplasma 64 (1967) 349-380
7. Cai S., Liu Y., Zheng Shu X., and Prestwich G.D. Injectable glycosaminoglycan hydrogels for controlled release of human basic fibroblast growth factor. Biomaterials 26 (2005) 6054-6067
8. Collinsworth A.M., Zhang S., Kraus W.E., and Truskey G.A. Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am. J. Physiol. Cell Physiol. 283 (2002) C1219-C1227
9. Dembo M., and Wang Y.-L. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76 (1999) 2307-2316
10. Dimitriadis E.K., Horkay F., Maresca J., Kachar B., and Chadwick R.S. Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 82 (2002) 2798-2810
11. Diridollou S., Patat F., Gens F., Vaillant L., Black D., Lagarde J.M., Gall Y., and Berson M. In vivo model of the mechanical properties of the human skin under suction. Skin. Res. Technol. 6 (2000) 214-221
12. Engler A., Bacakova L., Newman C., Hategan A., Griffin M., and Discher D. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86 (2004) 617-628
13. Engler A.J., Griffin M.A., Sen S., Bonnemann C.G., Sweeney H.L., and Discher D.E. Myotubes differentiate optimally on substrates with tissue-like stiffness: Pathological implications for soft or stiff microenvironments. J. Cell. Biol. 166 (2004) 877-887
14. Engler A.J., Richert L., Wong J.Y., Picart C., and Discher D.E. Surface probe measurements of the elasticity of sectioned tissue, thin gels and polyelectrolyte multilayer films: Correlations between substrate stiffness and cell adhesion. Surf. Sci. 570 (2004) 142-154
15. Engler A.J., Sen S., Sweeney H.L., and Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 126 (2006) 677-689
16. Firtel R.A. Integration of signaling information in controlling cell-fate decisions in dictyostelium. Genes Dev. 9 (1995) 1427-1444
17. Flanagan L.A., Ju Y.E., Marg B., Osterfield M., and Janmey P.A. Neurite branching on deformable substrates. Neuroreport 13 (2002) 2411-2415
18. Fung Y.-C. A First Course in Continuum Mechanics,. 3rd edn. (1994), Prentice-Hall, Englewood Cliffs, NJ
19. Gaudet C., Marganski W.A., Kim S., Brown C.T., Gunderia V., Dembo M., and Wong J.Y. Influence of type I collagen surface density on fibroblast spreading, motility, and contractility. Biophys. J. 85 (2003) 3329-3335
20. Gefen A., and Margulies S.S. Are in vivo and in situ brain tissues mechanically similar?. J. Biomech. 37 (2004) 1339-1352
21. Geissler E., Hecht A.M., Horkay F., and Zrinyi M. Compressional modulus of swollen polyacrylamide networks. Macromolecules 21 (1988) 2594-2599
22. Goffin J.M., Pittet P., Csucs G., Lussi J.W., Meister J.J., and Hinz B. Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J. Cell. Biol. 172 (2006) 259-268
23. Goldman R.D., Milsted A., Schloss J.A., Starger J., and Yerna M.J. Cytoplasmic fibers in mammalian cells: Cytoskeletal and contractile elements. Annu. Rev. Physiol. 41 (1979) 703-722
24. Harris A.K., Wild P., and Stopak D. Silicone rubber substrata: A new wrinkle in the study of cell locomotion. Science 208 (1980) 177-179
25. Hategan A., Law R., Kahn S., and Discher D.E. Adhesively-tensed cell membranes: Lysis kinetics and atomic force microscopy probing. Biophys. J. 85 (2003) 2746-2759
26. Hecht A.M., Duplessix R., and Geissler E. Structural inhomogeneities in the range 2.5-2500 A in polyacrylamide gels. Macromolecules 18 (1985) 2167-2173
27. Hermanson G. Bioconjuate Techniques. (1996), Academic Press, San Diego
28. Hertz H. Über die Berührung fester elastischer Körper. J. Reine Angew. Mathematik 92 (1882) 156-171
29. Jacot J.G., Dianis S., Schnall J., and Wong J.Y. A simple microindentation technique for mapping the microscale compliance of soft hydrated materials and tissues. J. Biomed. Mater. Res. A 79 (2006) 485-494
30. Kong H.J., Boontheekul T., and Mooney D.J. Quantifying the relation between adhesion ligand-receptor bond formation and cell phenotype. Proc. Natl. Acad. Sci. USA 103 (2006) 18534-18539
31. Kong H.J., Polte T.R., Alsberg E., and Mooney D.J. FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proc. Natl. Acad. Sci. USA 102 (2005) 4300-4305
32. Ladam G., Vonna L., and Sackmann E. Micromechanics of surface-grafted hyaluronic acid gels. J. Phys. Chem. B 107 (2003) 8965-8971
33. Li Y., Hu Z., and Li C. New method for measuring Poisson's ratio in polymer gels. J. Appl. Polymer. Sci. 50 (1993) 1107-1111
34. Lo C.M., Wang H.B., Dembo M., and Wang Y.L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79 (2000) 144-152
35. Mahaffy R.E., Shih C.K., MacKintosh F.C., and Kas J. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys. Rev. Lett. 85 (2000) 880-883
36. Oliver T., Dembo M., and Jacobson K. Traction forces in locomoting cells. Cell Motil. Cytoskeleton 31 (1995) 225-240
37. 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. Tensional homeostasis and the malignant phenotype. Cancer Cell 8 (2005) 241-254
38. Pelham R.J., and Wang Y.-L. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 94 (1997) 13661-13665
39. Peyton S.R., and Putnam A.J. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell. Physiol. 204 (2005) 198-209
40. Pollard T.D., Fujiwara K., Niederman R., and Maupin-Szamier P. Evidence for the role of cytoplasmic actin and myosin in cellular structure and motility. In: Goldman R., Pollard T., and Rosenbaum J. (Eds). "Cell Motility" (1976), Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 689-724
41. Radmacher M. Measuring the elastic properties of biological samples with the AFM. IEEE Eng. Med. Biol. Mag. 16 (1997) 47-57
42. Radmacher M., Fritz M., and Hansma P.K. Imaging soft samples with the atomic force microscope: Gelatin in water and propanol. Biophys. J. 69 (1995) 264-270
43. Rajagopalan P., Marganski W.A., Brown X.Q., and Wong J.Y. Direct comparison of the spread area, contractility, and migration of balb/c 3T3 fibroblasts adhered to fibronectin- and RGD-modified substrata. Biophys. J. 87 (2004) 2818-2827
44. Richert L., Engler A.J., Discher D.E., and Picart C. Elasticity of native and cross-linked polyelectrolyte multilayer films. Biomacromolecules 5 (2004) 1908-1916
45. Riveline D., Zamir E., Balaban N.Q., Schwarz U.S., Ishizaki T., Narumiya S., Kam Z., Geiger B., and Bershadsky A.D. Focal contacts as mechanosensors: Externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell. Biol. 153 (2001) 1175-1186
46. Rosenbluth M.J., Lam W.A., and Fletcher D.A. Force microscopy of nonadherent cells: A comparison of leukemia cell deformability. Biophys. J. 90 (2006) 2994-3003
47. Rotsch C., Jacobson K., and Radmacher M. Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc. Natl. Acad. Sci. USA 96 (1999) 921-926
48. Rotsch C., and Radmacher M. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophys. J. 78 (2000) 520-535
49. Saez A., Buguin A., Silberzan P., and Ladoux B. Is the mechanical activity of epithelial cells controlled by deformations or forces?. Biophys. J. 89 (2005) L52-L54
50. Schloss J.A., Milsted A., and Goldman R.D. Myosin subfragment binding for the localization of actin-like microfilaments in cultured cells. A light and electron microscope study. J. Cell. Biol. 74 (1977) 794-815
51. Sehgal D., and Vijay I.K. A method for the high efficiency of water-soluble carbodiimide-mediated amidation. Anal. Biochem. 218 (1994) 87-91
52. Sen S., Subramanian S., and Discher D.E. Indentation and adhesive probing of a cell membrane with AFM: Theoretical model and experiments. Biophys. J. 89 (2005) 3203-3213
53. Shu X.Z., Ahmad S., Liu Y., and Prestwich G.D. Synthesis and evaluation of injectable, in situ crosslinkable synthetic extracellular matrices for tissue engineering. J. Biomed. Mater. Res. A 79 (2006) 902-912
54. Shu X.Z., Liu Y.C., Luo Y., Roberts M.C., and Prestwich G.D. Disulfide cross-linked hyaluronan hydrogels. Biomacromolecules 3 (2002) 1304-1311
55. Sneddon I.N. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int. J. Eng. Sci. 3 (1965) 47-57
56. Storm C., Pastore J.J., MacKintosh F.C., Lubensky T.C., and Janmey P.A. Nonlinear elasticity in biological gels. Nature 435 (2005) 191-194
57. Wang N., Tolic-Norrelykke I.M., Chen J., Mijailovich S.M., Butler J.P., Fredberg J.J., and Stamenovic D. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Physiol. 282 (2002) C606-C616
58. Weisenhorn A.L., Hansma P.K., Albrecht T.R., and Quate C.F. Forces in atomic force microscopy in air and water. Appl. Phys. Lett. 54 (1989) 2651-2653
59. Yeung T., Georges P.C., Flanagan L.A., Marg B., Ortiz M., Funaki M., Zahir N., Ming W., Weaver V., and Janmey P.A. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60 (2005) 24-34