High-throughput ballistic injection nanorheology to measure cell mechanics

Nature Protocols

Volumn 7, Issue 1, 2012, Pages 155-170

  Wu, Pei Hsun ^a,b   Hale, Christopher M ^a,b   Chen, Wei Chiang ^a,b   Lee, Jerry S H ^a,c   Tseng, Yiider ^b,d   Wirtz, Denis ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; ARTICLE; CELL MOTION; CELL TRACKING; CELL TRANSPORT; CELL TYPE; CONTROLLED STUDY; FEMALE; FLOW KINETICS; HIGH THROUGHPUT BALLISTIC INJECTION NANORHEOLOGY; HUMAN; HUMAN CELL; MECHANICAL STRESS; PRIORITY JOURNAL; PROCESS OPTIMIZATION; SHEAR FLOW; VISCOELASTICITY;

ANIMALS; BIOMECHANICS; CAENORHABDITIS ELEGANS; CELLS, CULTURED; HUMANS; MICE; NANOPARTICLES; NANOTECHNOLOGY; RHEOLOGY; SWISS 3T3 CELLS; VISCOELASTIC SUBSTANCES;

ANIMALIA;

EID: 84861113455     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2011.436     Document Type: Article

References (72)

1. Hoh, J.H. & Schoenenberger, C.A. Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy. J. Cell. Sci. 107, 1105-1114 (1994). (Pubitemid 24177313)
2. Radmacher, M., Cleveland, J.P., Fritz, H.G., Hansma, H.G. & Hansma, P.K. Mapping interactions forces with the AFM. Biophys. J. 66, 2159-2165 (1994).
3. Domke, J., Parak, W.J., George, M., Gaub, H.E. & Radmacher, M. Mapping the mechanical pulse of single cardiomyocytes with the atomic force microscope. Eur. Biophys. J. 28, 179-186 (1999). (Pubitemid 29225595)
4. Radmacher, M. Studying the mechanics of cellular processes by atomic force microscopy. Methods Cell. Biol. 83, 347-372 (2007).
5. Hale, C.M., Sun, S.X. & Wirtz, D. Resolving the role of actoymyosin contractility in cell microrheology. PLoS ONE 4, e7054 (2009).
6. Daniels, B.R., Masi, B.C. & Wirtz, D. Probing single-cell micromechanics in vivo: the microrheology of C. elegans developing embryos. Biophys. J. 90, 4712-4719 (2006). (Pubitemid 43830915)
7. Lee, J.S. et al. Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fuid fow. J. Cell. Sci. 119, 1760-1768 (2006). (Pubitemid 43811002)
8. Panorchan, P., Lee, J.S., Kole, T.P., Tseng, Y. & Wirtz, D. Microrheology and ROCK signaling of human endothelial cells embedded in a 3D matrix. Biophys. J. 91, 3499-3507 (2006). (Pubitemid 44788283)
9. Zhou, X. et al. Fibronectin fbrillogenesis regulates three-dimensional neovessel formation. Genes Dev. 22, 1231-1243 (2008). (Pubitemid 351656581)
10. Lekka, M. & Laidler, P. Applicability of AFM in cancer detection. Nat. Nanotechnol. 4, 72; author reply 72-73 (2009).
11. Mason, T.G., Ganesan, K., van Zanten, J.V., Wirtz, D. & Kuo, S.C. Particle-tracking microrheology of complex fuids. Phys. Rev. Lett. 79, 3282-3285 (1997).
12. Wirtz, D. Particle-tracking microrheology of living cells: principles and applications. Annu. Rev. Biophys. 38, 301-326 (2009).
13. Wu, J. & Dai, L.L. Apparent microrheology of oil-water interfaces by single-particle tracking. Langmuir 23, 4324-4331 (2007). (Pubitemid 46643157)
14. Wilson, L.G., Harrison, A.W., Schofeld, A.B., Arlt, J. & Poon, W.C. Passive and active microrheology of hard-sphere colloids. J. Phys. Chem. B. 113, 3806-3812 (2009).
15. Vanapalli, S.A., Li, Y., Mugele, F. & Duits, M.H. On the origins of the universal dynamics of endogenous granules in mammalian cells. Mol. Cell. Biomech. 6, 191-201 (2009).
16. Sivaramakrishnan, S., DeGiulio, J.V., Lorand, L., Goldman, R.D. & Ridge, K.M. Micromechanical properties of keratin intermediate flament networks. Proc. Natl. Acad. Sci. USA 105, 889-894 (2008). (Pubitemid 351282051)
17. Silburn, S.A., Saunter, C.D., Girkin, J.M. & Love, G.D. Multidepth, multiparticle tracking for active microrheology using a smart camera. Rev. Sci. Instrum. 82, 033712 (2011).
18. Selvaggi, L. et al. Multiple-particle-tracking to investigate viscoelastic properties in living cells. Methods 51, 20-26 (2010).
19. Savin, T. & Doyle, P.S. Static and dynamic errors in particle tracking microrheology. Biophys. J. 88, 623-638 (2005). (Pubitemid 40070706)
20. Rogers, S.S., Waigh, T.A. & Lu, J.R. Intracellular microrheology of motile Amoeba proteus. Biophys. J. 94, 3313-3322 (2008).
21. Rogers, S.S., van der Walle, C. & Waigh, T.A. Microrheology of bacterial bioflms in vitro: Staphylococcus aureus and Pseudomonas aeruginosa. Langmuir 24, 13549-13555 (2008).
22. Rathgeber, S., Beauvisage, H.J., Chevreau, H., Willenbacher, N. & Oelschlaeger, C. Microrheology with fuorescence correlation spectroscopy. Langmuir 25, 6368-6376 (2009).
23. Papagiannopoulos, A., Waigh, T.A. & Hardingham, T.E. The viscoelasticity of self-assembled proteoglycan combs. Faraday Discuss. 139, 337-357; discussion 399-417, 419-420 (2008).
24. Papagiannopoulos, A., Fernyhough, C.M. & Waigh, T.A. The microrheology of polystyrene sulfonate combs in aqueous solution. J. Chem. Phys. 123, 214904 (2005).
25. Moschakis, T., Murray, B.S. & Dickinson, E. Particle tracking using confocal microscopy to probe the microrheology in a phase-separating emulsion containing nonadsorbing polysaccharide. Langmuir 22, 4710-4719 (2006). (Pubitemid 43829154)
26. Larsen, T.H. & Furst, E.M. Microrheology of the liquid-solid transition during gelation. Phys. Rev. Lett. 100, 146001 (2008).
27. Hasnain, I.A. & Donald, A.M. Microrheological characterization of anisotropic materials. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73, 031901 (2006).
28. Haro-Perez, C., Garcia-Castillo, A. & Arauz-Lara, J.L. Confnement-induced fuid-gel transition in polymeric solutions. Langmuir 25, 8911-8914 (2009).
29. del Alamo, J.C., Norwich, G.N., Li, Y.S., Lasheras, J.C. & Chien, S. Anisotropic rheology and directional mechanotransduction in vascular endothelial cells. Proc. Natl. Acad. Sci. USA 105, 15411-15416 (2008).
30. Crocker, J.C. & Hoffman, B.D. Multiple-particle tracking and two-point microrheology in cells. Methods Cell. Biol. 83, 141-178 (2007).
31. Corrigan, A.M. & Donald, A.M. Particle tracking microrheology of gel-forming amyloid fbril networks. Eur. Phys. J. E Soft Matter 28, 457-462 (2009).
32. Corrigan, A.M. & Donald, A.M. Passive microrheology of solvent-induced fbrillar protein networks. Langmuir 25, 8599-8605 (2009).
33. Baker, E.L., Lu, J., Yu, D., Bonnecaze, R.T. & Zaman, M.H. Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys. J. 99, 2048-2057 (2010).
34. Baker, E.L., Bonnecaze, R.T. & Zaman, M.H. Extracellular matrix stiffness and architecture govern intracellular rheology in cancer. Biophys. J. 97, 1013-1021 (2009).
35. Alam, M.M. & Mezzenga, R. Particle tracking microrheology of lyotropic liquid crystals. Langmuir 27, 6171-6178 (2011).
36. Addas, K.M., Schmidt, C.F. & Tang, J.X. Microrheology of solutions of semifexible biopolymer flaments using laser tweezers interferometry. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 70, 021503 (2004).
37. Tseng, Y., Kole, T.P. & Wirtz, D. Micromechanical mapping of live cells by multiple-particle-tracking microrheology. Biophys. J. 83, 3162-3176 (2002). (Pubitemid 36041936)
38. Kole, T.P., Tseng, Y. & Wirtz, D. Intracellular microrheology as a tool for the measurement of the local mechanical properties of live cells. Methods Cell. Biol. 78, 45-64 (2004).
39. Kole, T.P., Tseng, Y., Huang, L., Katz, J.L. & Wirtz, D. Rho kinase regulates the intracellular micromechanical response of adherent cells to rho activation. Mol. Biol. Cell. 15, 3475-3484 (2004). (Pubitemid 38850138)
40. Kole, T.P., Tseng, Y., Jiang, I., Katz, J.L. & Wirtz, D. Intracellular mechanics of migrating fbroblasts. Mol. Biol. Cell. 16, 328-338 (2005).
41. Gupton, S.L. et al. Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropomyosin. J. Cell. Biol. 168, 619-631 (2005). (Pubitemid 40271027)
42. Xu, J., Viasnoff, V. & Wirtz, D. Compliance of actin flament networks measured by particle-tracking microrheology and diffusing wave spectroscopy. Rheologica. Acta 37, 387-398 (1998).
43. Tseng, Y. et al. How actin crosslinking and bundling proteins cooperate to generate an enhanced cell mechanical response. Biochem. Biophys. Res. Commun. 334, 183-192 (2005). (Pubitemid 40978524)
44. Panorchan, P. et al. Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology. Methods Cell. Biol. 83, 115-140 (2007).
45. Lee, J.S. et al. Nuclear lamin A/C defciency induces defects in cell mechanics, polarization, and migration. Biophys. J. 93, 2542-2552 (2007). (Pubitemid 47511153)
46. Rufener, K., Palmer, A., Xu, J. & Wirtz, D. High-frequency dynamics and microrheology of macromolecular solutions measured by diffusing wave spectroscopy: the case of actin flament networks. J. NonNewtonian Fluid. Mech. 82, 303-314 (1999). (Pubitemid 29365912)
47. Mason, T.G., Dhople, A. & Wirtz, D. in Statistical Mechanics in Physics and Biology (eds. Wirtz, D. & Halsey, T.C.) 153-158 (Materials Research Society, 1997).
48. Mizuno, D., Tardin, C., Schmidt, C.F. & Mackintosh, F.C. Nonequilibrium mechanics of active cytoskeletal networks. Science 315, 370-373 (2007). (Pubitemid 46175516)
49. Lau, A.W., Hoffman, B.D., Davies, A., Crocker, J.C. & Lubensky, T.C. Microrheology, stress fuctuations, and active behavior of living cells. Phys. Rev. Lett. 91, 198101 (2003).
50. Hoffman, B.D., Massiera, G., Van Citters, K.M. & Crocker, J.C. The consensus mechanics of cultured mammalian cells. Proc. Natl. Acad. Sci. USA 103, 10259-10264 (2006). (Pubitemid 44051154)
51. Yamada, S., Wirtz, D. & Kuo, S.C. Mechanics of living cells measured by laser tracking microrheology. Biophys. J. 78, 1736-1747 (2000). (Pubitemid 30183572)
52. Spence, P., Gupta, V., Stephens, D.J. & Hudson, A.J. Optimising the precision for localising fuorescent proteins in living cells by 2D Gaussian ftting of digital images: application to COPII-coated endoplasmic reticulum exit sites. Eur. Biophys. J. 37, 1335-1349 (2008).
53. Crocker, J.C. & Grier, D.G. Methods of digital video microscopy for colloidal studies. J. Colloid Interface Sci. 179, 298-310 (1996). (Pubitemid 26172272)
54. Gonzalez, R.C. & Woods, R.E. Digital Image Processing (Prentice Hall, 2002).
55. Wu, P.H., Nelson, N. & Tseng, Y. A general method for improving spatial resolution by optimization of electron multiplication in CCD imaging. Opt. Express 18, 5199-5212 (2010).
56. Wu, P.H., Arce, S.H., Burney, P.R. & Tseng, Y. A novel approach to high accuracy of video-based microrheology. Biophys. J. 96, 5103-5111 (2009).
57. Savitzky, A. & Golay, M.J.E. Smoothing and differentiation of data by simplifed least squares procedures. Anal. Chem. 36, 1627-1639 (1964).
58. Qian, H., Sheetz, M.P. & Elson, E.L. Single particle tracking. Analysis of diffusion and fow in two-dimensional systems. Biophys. J. 60, 910-921 (1991).
59. Mason, T.G. Estimating the viscoelastic moduli of complex fuids using the generalized Stokes-Einstein equation. Rheologica. Acta 39, 371-378 (2000).
60. Dasgupta, B.R., Tee, S.-Y., Crocker, J.C., Friseken, B.J. & Weitz, D.A. Microrheology of polyethylene oxide using diffusing wave spectroscopy and single scattering. Phys. Rev. E 65, 051505 (2002).
61. Palmer, A., Xu, J. & Wirtz, D. High-frequency rheology of crosslinked actin networks measured by diffusing wave spectroscopy. Rheologica. Acta 37, 97-108 (1998).
62. Palmer, A., Xu, J., Kuo, S.C. & Wirtz, D. Diffusing wave spectroscopy microrheology of actin flament networks. Biophys. J. 76, 1063-1071 (1999). (Pubitemid 29264587)
63. Daniels, B.R. et al. Differences in the microrheology of human embryonic stem cells and human induced pluripotent stem cells. Biophys. J. 99, 3563-3570 (2010).
64. Hale, C.M. et al. Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys. J. 95, 5462-5475 (2008).
65. Stewart-Hutchinson, P.J., Hale, C.M., Wirtz, D. & Hodzic, D. Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp. Cell. Res. 314, 1892-1905 (2008).
66. Tseng, Y., Lee, J.S., Kole, T.P., Jiang, I. & Wirtz, D. Micro-organization and visco-elasticity of the interphase nucleus revealed by particle nanotracking. J. Cell. Sci. 117, 2159-2167 (2004). (Pubitemid 38745148)
67. Baker, E.L., Lu, J., Yu, D., Bonnecaze, R.T. & Zaman, M.H. Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys. J. 99, 2048-2057 (2010).
68. Rahman, A., Tseng, Y. & Wirtz, D. Micromechanical coupling between cell surface receptors and RGD peptides. Biochem. Biophys. Res. Commun. 296, 771-778 (2002).
69. Fire, A. Integrative transformation of Caenorhabditis elegans. EMBO J. 5, 2673-2680 (1986).
70. Panorchan, P., Tseng, Y. & Wirtz, D. Structure-function relationship of biological gels revealed by multiple particle tracking and differential interference contrast microscopy: The case of human lamin networks. Phys. Rev. E 70, 041906 (2004).
71. Fraley, S.I. et al. A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nat. Cell Biol. 12, 598-604 (2010).
72. Fraley, S.I., Feng, Y., Wirtz, D. & Longmore, G.D. Reply: reducing background fuorescence reveals adhesions in 3D matrices. Nat. Cell Biol. 13, 5-7 (2011).