Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy

Cell

Volumn 158, Issue 4, 2014, Pages 822-832

  Guo, Ming ^a   Ehrlicher, Allen J ^a,b,g   Jensen, Mikkel H ^a,c   Renz, Malte ^d   Moore, Jeffrey R ^c   Goldman, Robert D ^e   Lippincott Schwartz, Jennifer ^d   Mackintosh, Frederick C ^f   Weitz, David A ^a  

^a HARVARD UNIVERSITY   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c BOSTON UNIVERSITY   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

^f VU UNIVERSITY AMSTERDAM   (Netherlands)

^g MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

VIMENTIN; PROTEIN;

ARTICLE; CELL FUNCTION; CELL MOTION; CELL ORGANELLE; CONTROLLED STUDY; CYTOPLASM; FORCE SPECTRUM MICROSCOPY; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MICROSCOPY; MOTOR ACTIVITY; PRIORITY JOURNAL; STOCHASTIC MODEL; ANIMAL; ANIMAL EMBRYO; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CHEMISTRY; CYTOLOGY; FIBROBLAST; MOUSE; PROCEDURES;

ANIMALS; BIOMECHANICAL PHENOMENA; CYTOPLASM; EMBRYO, MAMMALIAN; FIBROBLASTS; MICE; MICROSCOPY, ATOMIC FORCE; PROTEINS; VIMENTIN;

EID: 84907369302     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.06.051     Document Type: Article

References (59)

1. D.B. Agus, J.F. Alexander, W. Arap, S. Ashili, J.E. Aslan, R.H. Austin, V. Backman, K.J. Bethel, R. Bonneau, W.C. Chen Physical Sciences - Oncology Centers Network A physical sciences network characterization of non-tumorigenic and metastatic cells Sci Rep 3 2013 1449
2. V. Ananthanarayanan, M. Schattat, S.K. Vogel, A. Krull, N. Pavin, and I.M. Tolić-Nørrelykke Dynein motion switches from diffusive to directed upon cortical anchoring Cell 153 2013 1526 1536
3. E.L. Baker, J. Lu, D.H. Yu, R.T. Bonnecaze, and M.H. Zaman Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential Biophys. J. 99 2010 2048 2057
4. C.P. Brangwynne, G.H. Koenderink, F.C. MacKintosh, and D.A. Weitz Cytoplasmic diffusion: molecular motors mix it up J. Cell Biol. 183 2008 583 587
5. C.P. Brangwynne, G.H. Koenderink, F.C. Mackintosh, and D.A. Weitz Nonequilibrium microtubule fluctuations in a model cytoskeleton Phys. Rev. Lett. 100 2008 118104
6. P. Bursac, G. Lenormand, B. Fabry, M. Oliver, D.A. Weitz, V. Viasnoff, J.P. Butler, and J.J. Fredberg Cytoskeletal remodelling and slow dynamics in the living cell Nat. Mater. 4 2005 557 561
7. S.W. Chan, C.J. Lim, K. Guo, C.P. Ng, I. Lee, W. Hunziker, Q. Zeng, and W.J. Hong A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells Cancer Res. 68 2008 2592 2598
8. D.M. Chudakov, S. Lukyanov, and K.A. Lukyanov Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2 Nat. Protoc. 2 2007 2024 2032
9. S.E. Cross, Y.S. Jin, J. Rao, and J.K. Gimzewski Nanomechanical analysis of cells from cancer patients Nat. Nanotechnol. 2 2007 780 783
10. C.C. Cunningham, J.B. Gorlin, D.J. Kwiatkowski, J.H. Hartwig, P.A. Janmey, H.R. Byers, and T.P. Stossel Actin-binding protein requirement for cortical stability and efficient locomotion Science 255 1992 325 327
11. R.J. Deberardinis, N. Sayed, D. Ditsworth, and C.B. Thompson Brick by brick: metabolism and tumor cell growth Curr. Opin. Genet. Dev. 18 2008 54 61
12. J.C. del Alamo, G.N. Norwich, Y.S.J. Li, J.C. Lasheras, and S. Chien Anisotropic rheology and directional mechanotransduction in vascular endothelial cells Proc. Natl. Acad. Sci. USA 105 2008 15411 15416
13. A.D. Doyle, and K.M. Yamada Cell biology: Sensing tension Nature 466 2010 192 193
14. Y.F. Dufrêne, E. Evans, A. Engel, J. Helenius, H.E. Gaub, and D.J. Müller Five challenges to bringing single-molecule force spectroscopy into living cells Nat. Methods 8 2011 123 127
15. A.J. Ehrlicher, F. Nakamura, J.H. Hartwig, D.A. Weitz, and T.P. Stossel Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A Nature 478 2011 260 263
16. B. Fabry, G.N. Maksym, J.P. Butler, M. Glogauer, D. Navajas, and J.J. Fredberg Scaling the microrheology of living cells Phys. Rev. Lett. 87 2001 148102
17. C. Grashoff, B.D. Hoffman, M.D. Brenner, R.B. Zhou, M. Parsons, M.T. Yang, M.A. McLean, S.G. Sligar, C.S. Chen, T. Ha, and M.A. Schwartz Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 466 2010 263 266
18. G.G. Gundersen, and H.J. Worman Nuclear positioning Cell 152 2013 1376 1389
19. M. Guo, A.J. Ehrlicher, S. Mahammad, H. Fabich, M.H. Jensen, J.R. Moore, J.J. Fredberg, R.D. Goldman, and D.A. Weitz The role of vimentin intermediate filaments in cortical and cytoplasmic mechanics Biophys. J. 105 2013 1562 1568
20. S.L. Gupton, K.L. Anderson, T.P. Kole, R.S. Fischer, A. Ponti, S.E. Hitchcock-DeGregori, G. Danuser, V.M. Fowler, D. Wirtz, D. Hanein, and C.M. Waterman-Storer Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropomyosin J. Cell Biol. 168 2005 619 631
21. C.M. Hale, S.X. Sun, and D. Wirtz Resolving the role of actoymyosin contractility in cell microrheology PLoS ONE 4 2009 e7054
22. P. Hammar, P. Leroy, A. Mahmutovic, E.G. Marklund, O.G. Berg, and J. Elf The lac repressor displays facilitated diffusion in living cells Science 336 2012 1595 1598
23. W.P. Han, Y.K. Ng, D. Axelrod, and E.S. Levitan Neuropeptide release by efficient recruitment of diffusing cytoplasmic secretory vesicles Proc. Natl. Acad. Sci. USA 96 1999 14577 14582
24. C.-P. Heisenberg, and Y. Bellaïche Forces in tissue morphogenesis and patterning Cell 153 2013 948 962
25. A.G. Hendricks, E.L.F. Holzbaur, and Y.E. Goldman Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors Proc. Natl. Acad. Sci. USA 109 2012 18447 18452
26. B.D. Hoffman, G. Massiera, K.M. Van Citters, and J.C. Crocker The consensus mechanics of cultured mammalian cells Proc. Natl. Acad. Sci. USA 103 2006 10259 10264
27. R.G. Holzer, C. MacDougall, G. Cortright, K. Atwood, J.E. Green, and C.L. Jorcyk Development and characterization of a progressive series of mammary adenocarcinoma cell lines derived from the C3(1)/SV40 Large T-antigen transgenic mouse model Breast Cancer Res. Treat. 77 2003 65 76
28. J. Howard Mechanics of motor proteins and the cytoskeleton 2001 Sinauer Associates Sunderland, MA
29. K. Jaqaman, H. Kuwata, N. Touret, R. Collins, W.S. Trimble, G. Danuser, and S. Grinstein Cytoskeletal control of CD36 diffusion promotes its receptor and signaling function Cell 146 2011 593 606
30. G.H. Koenderink, Z. Dogic, F. Nakamura, P.M. Bendix, F.C. MacKintosh, J.H. Hartwig, T.P. Stossel, and D.A. Weitz An active biopolymer network controlled by molecular motors Proc. Natl. Acad. Sci. USA 106 2009 15192 15197
31. M. Kovács, J. Tóth, C. Hetényi, A. Málnási-Csizmadia, and J.R. Sellers Mechanism of blebbistatin inhibition of myosin II J. Biol. Chem. 279 2004 35557 35563
32. C.M. Kraning-Rush, J.P. Califano, and C.A. Reinhart-King Cellular traction stresses increase with increasing metastatic potential PLoS ONE 7 2012 e32572
33. M. Kyoung, and E.D. Sheets Vesicle diffusion close to a membrane: intermembrane interactions measured with fluorescence correlation spectroscopy Biophys. J. 95 2008 5789 5797
34. A.W.C. Lau, B.D. Hoffman, A. Davies, J.C. Crocker, and T.C. Lubensky Microrheology, stress fluctuations, and active behavior of living cells Phys. Rev. Lett. 91 2003 198101
35. K. Luby-Phelps Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area Int. Rev. Cytol. 192 2000 189 221
36. K. Luby-Phelps, P.E. Castle, D.L. Taylor, and F. Lanni Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells Proc. Natl. Acad. Sci. USA 84 1987 4910 4913
37. F.C. MacKintosh Active diffusion: the erratic dance of chromosomal loci Proc. Natl. Acad. Sci. USA 109 2012 7138 7139
38. F.C. MacKintosh, and A.J. Levine Nonequilibrium mechanics and dynamics of motor-activated gels Phys. Rev. Lett. 100 2008 018104
39. M.G. Mendez, S.I. Kojima, and R.D. Goldman Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition FASEB J. 24 2010 1838 1851
40. D. Mizuno, C. Tardin, C.F. Schmidt, and F.C. Mackintosh Nonequilibrium mechanics of active cytoskeletal networks Science 315 2007 370 373
41. D. Mizuno, R. Bacabac, C. Tardin, D. Head, and C.F. Schmidt High-resolution probing of cellular force transmission Phys. Rev. Lett. 102 2009 168102
42. G.M. Nagaraja, M. Othman, B.P. Fox, R. Alsaber, C.M. Pellegrino, Y. Zeng, R. Khanna, P. Tamburini, A. Swaroop, and R.P. Kandpal Gene expression signatures and biomarkers of noninvasive and invasive breast cancer cells: comprehensive profiles by representational difference analysis, microarrays and proteomics Oncogene 25 2006 2328 2338
43. B.R. Parry, I.V. Surovtsev, M.T. Cabeen, C.S. O'Hern, E.R. Dufresne, and C. Jacobs-Wagner The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity Cell 156 2014 183 194
44. M. Plodinec, M. Loparic, C.A. Monnier, E.C. Obermann, R. Zanetti-Dallenbach, P. Oertle, J.T. Hyotyla, U. Aebi, M. Bentires-Alj, and C.A. Schoenenberger et al. The Nanomechanical Signature of Breast Cancer Biophys. J. 104 2013 321A-321A
45. A.K. Rai, A. Rai, A.J. Ramaiya, R. Jha, and R. Mallik Molecular adaptations allow dynein to generate large collective forces inside cells Cell 152 2013 172 182
46. C.J. Sherr Cancer cell cycles Science 274 1996 1672 1677
47. K. Svoboda, and S.M. Block Force and velocity measured for single kinesin molecules Cell 77 1994 773 784
48. R.D. Vale The molecular motor toolbox for intracellular transport Cell 112 2003 467 480
49. M.T. Valentine, Z.E. Perlman, M.L. Gardel, J.H. Shin, P. Matsudaira, T.J. Mitchison, and D.A. Weitz Colloid surface chemistry critically affects multiple particle tracking measurements of biomaterials Biophys. J. 86 2004 4004 4014
50. C. Veigel, M.L. Bartoo, D.C.S. White, J.C. Sparrow, and J.E. Molloy The stiffness of rabbit skeletal actomyosin cross-bridges determined with an optical tweezers transducer Biophys. J. 75 1998 1424 1438
51. X. Wang, and T.L. Schwarz The mechanism of Ca2+ -dependent regulation of kinesin-mediated mitochondrial motility Cell 136 2009 163 174
52. S.C. Weber, A.J. Spakowitz, and J.A. Theriot Nonthermal ATP-dependent fluctuations contribute to the in vivo motion of chromosomal loci Proc. Natl. Acad. Sci. USA 109 2012 7338 7343
53. C. Wilhelm Out-of-equilibrium microrheology inside living cells Phys. Rev. Lett. 101 2008 028101
54. P.H. Wu, C.M. Hale, W.C. Chen, J.S.H. Lee, Y. Tseng, and D. Wirtz High-throughput ballistic injection nanorheology to measure cell mechanics Nat. Protoc. 7 2012 155 170
55. S. Yamada, D. Wirtz, and S.C. Kuo Mechanics of living cells measured by laser tracking microrheology Biophys. J. 78 2000 1736 1747
56. E.H. Zhou, X. Trepat, C.Y. Park, G. Lenormand, M.N. Oliver, S.M. Mijailovich, C. Hardin, D.A. Weitz, J.P. Butler, and J.J. Fredberg Universal behavior of the osmotically compressed cell and its analogy to the colloidal glass transition Proc. Natl. Acad. Sci. USA 106 2009 10632 10637
57. D.M. Chudakov, S. Lukyanov, and K.A. Lukyanov Using photoactivatable fluorescent protein Dendra2 to track protein movement Biotechniques 42 2007 553, 555, 557 passim
58. J. Liu, Z.G. Pei, L.A. Wang, Z.H. Zhang, S.Q. Zeng, and Z.L. Huang A straightforward and quantitative approach for characterizing the photoactivation performance of optical highlighter fluorescent proteins Appl. Phys. Lett. 97 2010 203701
59. A.F. Straight, A. Cheung, J. Limouze, I. Chen, N.J. Westwood, J.R. Sellers, and T.J. Mitchison Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor Science 299 2003 1743 1747