Cellular and Nuclear Forces: An Overview

  • Bidisha Sinha
  • Arikta Biswas
  • Gautam V. Soni
Part of the Methods in Molecular Biology book series (MIMB, volume 1805)


Biological cells sample their surrounding microenvironments using nanoscale force sensors on the cell surfaces. These surface-based force and stress sensors generate physical and chemical responses inside the cell. The inherently well-connected cytoskeleton and its physical contacts with the force elements on the nuclear membrane lead these physicochemical responses to cascade all the way inside the cell nucleus, physically altering the nuclear state. These physical alterations of the cell nucleus, through yet-unknown complex steps elicit physical and functional response from the chromatin in the form of altered gene expression profiles. This mechanism of force/stress sensing by the cell and then its nuclear response has been shown to play a vital role in maintaining robust cellular homeostasis, controlling gene expression profiles during developmental phases as well as cell differentiation. Over the last few years, there has been appreciable progress toward identification of the molecular players responsible for force sensing. However, the actual sensing mechanism of cell surface bound force sensors and more importantly cascading of the signals, both physical (via cytosolic force sensing elements such as microtubule and actin framework) and chemical (cascade of biochemical signaling from cell surface to nuclear surface and further to the chromatin), inside the cell is poorly understood. In this chapter, we present a review of the currently known molecular players in cellular as well as nuclear force sensing repertoire and their possible mechanistic aspects. We also introduce various biophysical concepts that are used to describe the force/stress sensing and response of a cell. We hope this will help asking clearer questions and designing pointed experiments for better understanding of the force-dependent design principles of the cell surface, nuclear surface, and gene expression.

Key words

Nuclear mechanics Microrheology Membrane tension Actomyosin cortex Traction stress Cell–cell adhesion 


  1. 1.
    Ananthakrishnan R, Ehrlicher A (2007) The forces behind cell movement. Int J Biol Sci 3:303–317PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Kumar S, Weaver VM (2009) Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 28:113–127PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Heisenberg C-P, Bellaïche Y (2013) Forces in tissue morphogenesis and patterning. Cell 153:948–962PubMedCrossRefGoogle Scholar
  4. 4.
    Mayor S, Koster DV (2016) Cortical actin and the plasma membrane: inextricably intertwined. Curr Opin Cell Biol 38:81–89PubMedCrossRefGoogle Scholar
  5. 5.
    Ellis RJ (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 11:114–119PubMedCrossRefGoogle Scholar
  6. 6.
    Guo M et al (2014) Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy. Cell 158:822–832PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Fakhri N et al (2014) High-resolution mapping of intracellular fluctuations using carbon nanotubes. Science 344(6187):1031–1035PubMedCrossRefGoogle Scholar
  8. 8.
    Wagner O, Zinke J, Dancker P, Grill W, Bereiter-Hahn J (1999) Viscoelastic properties of f-actin, microtubules, f-actin/alpha-actinin, and f-actin/hexokinase determined in microliter volumes with a novel nondestructive method. Biophys J 76:2784–2796PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Bustamante C, Chemla YR, Forde NR, Izhaky D (2004) Mechanical processes in biochemistry. Annu Rev Biochem 73:705–748PubMedCrossRefGoogle Scholar
  10. 10.
    Sinha DK, Bhalla US, Shivashankar GV (2004) Kinetic measurement of ribosome motor stalling force. Appl Phys Lett 85:4789–4791CrossRefGoogle Scholar
  11. 11.
    Marenduzzo D, Finan K, Cook PR (2006) The depletion attraction: an underappreciated force driving cellular organization. J Cell Biol 175:681–686PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Kegel WK, Schoot Pv P (2004) Competing hydrophobic and screened-coulomb interactions in hepatitis B virus capsid assembly. Biophys J 86:3905–3913PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Goldberg M, Harel A, Gruenbaum Y (1999) The nuclear lamina: molecular organization and interaction with chromatin. Crit Rev Eukaryot Gene Expr 9:285–293PubMedCrossRefGoogle Scholar
  14. 14.
    Charras GT, Yarrow JC, Horton MA, Mahadevan L, Mitchison TJ (2011) Non-equilibration of hydrostatic pressure in blebbing cells. Nature 4:365–369Google Scholar
  15. 15.
    Stroka KM et al (2014) Water permeation drives tumor cell migration in confined microenvironments. Cell 157:611–623PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Charras GT, Coughlin M, Mitchison TJ, Mahadevan L (2008) Life and times of a cellular bleb. Biophys J 94:1836–1853PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Nelson P (2008) Biological physics-energy, information, life. W. H. Freeman and Company, New York. CrossRefGoogle Scholar
  18. 18.
    Morris CE, Homann U (2001) Cell surface area regulation and membrane tension. Membr Biol 179:79–102CrossRefGoogle Scholar
  19. 19.
    Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193–276PubMedCrossRefGoogle Scholar
  20. 20.
    Miermont A et al (2013) Severe osmotic compression triggers a slowdown of intracellular signaling, which can be explained by molecular crowding. Proc Natl Acad Sci U S A 110:5725–5730PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    de Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12:833–845PubMedCrossRefGoogle Scholar
  22. 22.
    Mitchell MJ, King MR (2013) Computational and experimental models of cancer cell response to fluid shear stress. Front Oncol 3:44PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Turitto VT (1982) Blood viscosity, mass transport, and thrombogenesis. Prog Hemost Thromb 6:139–177PubMedGoogle Scholar
  24. 24.
    Malek AM et al (1999) Hemodynamic shear stress and its role in atherosclerosis. JAMA 282:2035PubMedCrossRefGoogle Scholar
  25. 25.
    Boyd NL et al (2003) Chronic shear induces caveolae formation and alters ERK and Akt responses in endothelial cells. Am J Physiol Heart Circ Physiol 285:H1113–H1122PubMedCrossRefGoogle Scholar
  26. 26.
    Noria S et al (2004) Assembly and reorientation of stress Fibers drives morphological changes to endothelial cells exposed to shear stress. Am J Pathol 164:1211–1223PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Balaban NQ et al (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 3:466–472PubMedCrossRefGoogle Scholar
  28. 28.
    Buxboim A, Ivanovska IL, Discher DE (2010) Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells ‘feel’ outside and in? J Cell Sci 123:297–308PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Nemir S, West JL (2010) Synthetic materials in the study of cell response to substrate rigidity. Ann Biomed Eng 38:2–20PubMedCrossRefGoogle Scholar
  30. 30.
    Lo C-M, Wang H-B, Dembo M, Wang Y (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79:144–152PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Rape AD, Guo W-H, Wang Y-L (2011) The regulation of traction force in relation to cell shape and focal adhesions. Biomaterials 32:2043–2051PubMedCrossRefGoogle Scholar
  32. 32.
    Burton K, Park JH, Taylor DL (1999) Keratocytes generate traction forces in two phases. Mol Biol Cell 10:3745–3769PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Galbraith CG, Sheetz MP (1997) A micromachined device provides a new bend on fibroblast traction forces. Proc Natl Acad Sci U S A 94:9114–9118PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Yeung T et al (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60:24–34PubMedCrossRefGoogle Scholar
  35. 35.
    Borghi N et al (2012) E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc Natl Acad Sci U S A 109:12568–12573PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Harris AR, Daeden A, Charras GT (2014) Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers. J Cell Sci 127:2507–2517PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Lee LM, Liu AP (2014) The application of micropipette aspiration in molecular mechanics of single cells. J Nanotechnol Eng Med 5:0408011–0408016PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Sheetz MP, Dai J (1996) Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol 6:85–89PubMedCrossRefGoogle Scholar
  39. 39.
    Dimova R (2014) Recent developments in the field of bending rigidity measurements on membranes. Adv Colloid Interf Sci 208:225–234CrossRefGoogle Scholar
  40. 40.
    Neuman KC, Nagy A (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods 5:491–505PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Alert R, Casademunt J, Brugués J, Sens P (2015) Model for probing membrane-cortex adhesion by micropipette aspiration and fluctuation spectroscopy. Biophys J 108:1878–1886PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Sens P, Plastino J (2015) Membrane tension and cytoskeleton organization in cell motility. J Phys Condens Matter 273103(13 pp):27Google Scholar
  43. 43.
    Römer W et al (2007) Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 450:670–675PubMedCrossRefGoogle Scholar
  44. 44.
    Morris CE, Homann U (2001) Membrane biology cell surface area regulation and membrane tension. J Membr Biol 102:79–102CrossRefGoogle Scholar
  45. 45.
    Lieber AD, Schweitzer Y, Kozlov MM, Keren K (2015) Front-to-rear membrane tension gradient in rapidly moving cells. Biophys J 108:1599–1603PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Martinac B (2004) Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci 117:2449–2460PubMedCrossRefGoogle Scholar
  47. 47.
    Simunovic M, Voth GA, Callan-Jones A, Bassereau P (2015) When physics takes over: BAR proteins and membrane curvature physics of protein–membrane assemblies at large scales: beyond a structural description. Trends Cell Biol 25:780–792PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Mogilner A, Rubinstein B (2005) The physics of Filopodial protrusion. Biophys J 89:782–795PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Weichsel J, Schwarz US, Bioquant A, Mogilner A (2010) Two competing orientation patterns explain experimentally observed anomalies in growing actin networks. Proc Natl Acad Sci U S A 107:6304–6309PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Carlsson AE, Bayly PV (2014) Force generation by Endocytic actin patches in budding yeast. Biophys J 106:1596–1606PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Holmes CK, Popp D, Gebhard W, Kabsch W (1990) Atomic model of the actin filament. Nature 347:44–49PubMedCrossRefGoogle Scholar
  52. 52.
    Zhu J et al (2012) Mesoscopic model of actin-based propulsion. PLoS Comput Biol 8:e1002764PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Dmitrieff S, Nédélec F (2016) Amplification of actin polymerization forces. J Cell Biol 212:763–766PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Pollard TD (1986) Rate constants for the reactions of ATP-and ADP-actin with the ends of actin filaments. J Cell Biol 103:2747PubMedCrossRefGoogle Scholar
  55. 55.
    Dogterom M, Yurke B (1997) Measurement of the force-velocity relation for growing microtubules. Science 278:856–859PubMedCrossRefGoogle Scholar
  56. 56.
    Kerssemakers JWJ et al (2006) Assembly dynamics of microtubules at molecular resolution. Nature 442:709–712PubMedCrossRefGoogle Scholar
  57. 57.
    Nedelec F, Surrey T, Karsenti E (2003) Self-organization and forces in the microtubule cytoskeleton. Curr Opin Cell Biol 15:118–124PubMedCrossRefGoogle Scholar
  58. 58.
    Wittmann T, Hyman A, Desai A (2001) The spindle: a dynamic assembly of microtubules and motors. Nat Cell Biol 3:E28–E34PubMedCrossRefGoogle Scholar
  59. 59.
    Tran PT, Marsh L, Doye V, Inoue S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153:397–411PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Blanchoin L, Boujemaa-Paterski R, Sykes C, Plastino J (2014) Actin dynamics, architecture, and mechanics in cell motility. Physiol Rev 94:235–263. CrossRefPubMedGoogle Scholar
  61. 61.
    Murrell M, Oakes PW, Lenz M, Gardel ML (2015) Forcing cells into shape: the mechanics of actomyosin contractility. Nat Rev Mol Cell Biol 16:486–498PubMedCrossRefGoogle Scholar
  62. 62.
    Fernandez-Gonzalez R et al (2009) Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 17:736–743PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Lecuit T, Lenne P-F (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8:633–644PubMedCrossRefGoogle Scholar
  64. 64.
    Salbreux G, Charras G, Paluch E (2012) Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol 22:536–545PubMedCrossRefGoogle Scholar
  65. 65.
    Clark AG, Wartlick O, Salbreux G, Paluch EK (2014) Stresses at the cell surface during animal cell morphogenesis. Curr Biol 24:R484–R494PubMedCrossRefGoogle Scholar
  66. 66.
    Yumura S (2001) Myosin II dynamics and cortical flow during contractile ring formation in Dictyostelium cells. J Cell Biol 154:137–145PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Uehara R et al (2010) Determinants of myosin II cortical localization during cytokinesis. Curr Biol 20:1080–1085PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Guha M, Zhou M, Wang Y-L (2005) Cortical actin turnover during cytokinesis requires myosin II. Curr Biol 15:732–736PubMedCrossRefGoogle Scholar
  69. 69.
    Murthy K, Wadsworth P (2005) Myosin-II-dependent localization and dynamics of F-actin during cytokinesis. Curr Biol 15:724–731PubMedCrossRefGoogle Scholar
  70. 70.
    Mukhina S, Wang Y-L, Murata-Hori M (2007) Alpha-actinin is required for tightly regulated remodeling of the actin cortical network during cytokinesis. Dev Cell 13:554–565PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Reichl EM et al (2008) Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics. Curr Biol 18:471–480PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Fritzsche M, Lewallea A, Dukea T, Krusec K, Charras G (2013) Analysis of turnover dynamics of the submembranous actin cortex. Mol Biol Cell 24:757–767PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Volkmer Ward SM, Weins A, Pollak MR, Weitz DA (2008) Dynamic viscoelasticity of actin cross-linked with wild-type and disease-causing mutant a-Actinin-4. Biophys J 95:4915–4923CrossRefGoogle Scholar
  74. 74.
    Xu J, Tseng Y, Wirtz D (2000) Strain hardening of actin filament networks. J Biol Chem 275:35886–35892PubMedCrossRefGoogle Scholar
  75. 75.
    Bustamante C, Bryant Z, Smith SB (2003) Ten years of tension: single-molecule DNA mechanics. Nature 421:423–427PubMedCrossRefGoogle Scholar
  76. 76.
    Morton NE (1991) Parameters of the human genome. Proc Natl Acad Sci U S A 88:7474–7476PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Grewal SIS, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8:35–46PubMedCrossRefGoogle Scholar
  78. 78.
    Humphrey JD, Dufresne ER, Schwartz MA (2014) Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 15:802–812PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Isermann P, Lammerding J (2013) Nuclear mechanics and mechanotransduction in health and disease. Curr Biol 23:R1113–R1121PubMedCrossRefGoogle Scholar
  80. 80.
    Strambio-De-Castillia C, Niepel M, Rout MP (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 11:490–501PubMedCrossRefGoogle Scholar
  81. 81.
    Belaadi N, Aureille J, Guilluy C (2016) Under pressure: mechanical stress Management in the Nucleus. Cell 5:27CrossRefGoogle Scholar
  82. 82.
    Guilluy C, Burridge K (2015) Nuclear mechanotransduction: forcing the nucleus to respond. Nucleus 6:19–22PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Shivashankar GV (2011) Mechanosignaling to the cell nucleus and gene regulation. Annu Rev Biophys 40:361–378PubMedCrossRefGoogle Scholar
  84. 84.
    Pederson T, Marko JF (2014) Nuclear physics (of the cell, not the atom). Mol Biol Cell 25:3466–3469PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Alam S, Lovett DB, Dickinson RB, Roux KJ, Lele TP (2014) Nuclear forces and cell mechanosensing. Prog Mol Biol Transl Sci 126:205–215PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Dickinson RB, Neelam S, Lele TP (2015) Dynamic, mechanical integration between nucleus and cell- where physics meets biology. Nucleus 6:360–365PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Spagnol ST, Armiger TJ, Dahl KN (2016) Mechanobiology of chromatin and the nuclear interior. Cell Mol Bioeng.
  88. 88.
    Bronshtein I et al (2016) Exploring chromatin organization mechanisms through its dynamic properties. Nucleus 7:27–33PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Lavelle C (2014) Pack, unpack, bend, twist, pull, push: the physical side of gene expression. Curr Opin Genet Dev 25:74–84PubMedCrossRefGoogle Scholar
  90. 90.
    Mozziconacci J, Lavelle C (2008) Chromatin Fiber: 30 years of models. DNA Seq 1953:1–17Google Scholar
  91. 91.
    Mammoto A, Mammoto T, Ingber DE (2012) Mechanosensitive mechanisms in transcriptional regulation. J Cell Sci 125:3061–3073PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Dahl KN, Kalinowski A (2011) Nucleoskeleton mechanics at a glance. J Cell Sci 124:675–678PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Simon DN, Wilson KL (2011) The nucleoskeleton as a genome-associated dynamic ‘network of networks. Nat Rev Mol Cell Biol 12:695–708PubMedCrossRefGoogle Scholar
  94. 94.
    Ahmed S, Brickner JH (2007) Regulation and epigenetic control of transcription at the nuclear periphery. Trends Genet 23:396–402PubMedCrossRefGoogle Scholar
  95. 95.
    Towbin BD, Meister P, Gasser SM (2009) The nuclear envelope–a scaffold for silencing? Curr Opin Genet Dev 19:180–186PubMedCrossRefGoogle Scholar
  96. 96.
    Schäpe J, Prauße S, Radmacher M, Stick R (2009) Influence of Lamin a on the mechanical properties of amphibian oocyte nuclei measured by atomic force microscopy. Biophys J 96:4319–4325PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Aebi U, Cohn J, Buhle L, Gerace L (1986) The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323:560–564PubMedCrossRefGoogle Scholar
  98. 98.
    Coffinier C, Fong LG, Young SG (2010) LINCing Lamin B2 to neuronal migration: growing evidence for cell-specific roles of B-type lamins. Nucleus 1:407–411PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Young SG, Jung HJ, Coffinier C, Fong LG (2012) Understanding the roles of nuclear A- and B-type lamins in brain development. J Biol Chem 287:16103–16110PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Dahl KN, Kahn SM, Wilson KL, Discher DE (2004) The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J Cell Sci 117:4779–4786PubMedCrossRefGoogle Scholar
  101. 101.
    Schirmer EC, Foisner R (2007) Proteins that associate with lamins: many faces, many functions. Exp Cell Res 313:2167–2179PubMedCrossRefGoogle Scholar
  102. 102.
    Dechat T et al (2008) Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22:832–853PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Pederson T, Aebi U (2002) Actin in the nucleus: what form and what for? J Struct Biol 140:3–9PubMedCrossRefGoogle Scholar
  104. 104.
    Young KG, Kothary R (2005) Spectrin repeat proteins in the nucleus. BioEssays 27:144–152PubMedCrossRefGoogle Scholar
  105. 105.
    Zhong Z, Wilson KL, Dahl KN (2010) Beyond lamins other structural components of the nucleoskeleton. Methods Cell Biol 98:97–119PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Zastrow MS, Flaherty DB, Benian GM, Wilson KL (2006) Nuclear titin interacts with A- and B-type lamins in vitro and in vivo. J Cell Sci 119:239–249PubMedCrossRefGoogle Scholar
  107. 107.
    Wagner N, Krohne G (2007) LEM-domain proteins: new insights into Lamin-interacting proteins. Int Rev Cytol 261:1–46PubMedCrossRefGoogle Scholar
  108. 108.
    Swift J et al (2014) The nuclear lamina is mechano-responsive to ECM elasticity in mature tissue. J Cell Sci 127:3005–3015PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Torbati M, Lele TP, Agrawal A (2016) An unresolved LINC in the nuclear envelope. Cell Mol Bioeng 9:1–6CrossRefGoogle Scholar
  110. 110.
    Uzer G, Rubin CT, Rubin J (2016) Cell Mechanosensitivity is enabled by the LINC nuclear complex. Curr Mol Biol Rep 2:36–47PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Meinke P, Schirmer EC (2015) LINC’ing form and function at the nuclear envelope. FEBS Lett 589:2514–2521PubMedCrossRefGoogle Scholar
  112. 112.
    Lombardi ML, Lammerding J (2011) Keeping the LINC: the importance of nucleo-cytoskeletal coupling in intracellular force transmission and cellular function. Biochem Soc Trans 39:1729–1734PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Lombardi ML et al (2011) The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 286:26743–26753PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Friedl P, Wolf K, Lammerding J (2011) Nuclear mechanics during cell migration. Curr Opin Cell Biol 23:55–64PubMedCrossRefGoogle Scholar
  115. 115.
    Chancellory TJ, Lee J, Thodeti CK, Lele T (2010) Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys J 99:115–123CrossRefGoogle Scholar
  116. 116.
    Alam SG et al (2015) The nucleus is an intracellular propagator of tensile forces in NIH 3T3 fibroblasts. J Cell Sci 128:1901–1911PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Starr DA, Fridolfsson HN (2010) Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26:421–444PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Sosa BA, Kutay U, Schwartz TU (2013) Structural insights into LINC complexes. Curr Opin Struct Biol 23:285–291PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Chang W, Worman HJ, Gundersen GG (2015) Accessorizing and anchoring the LINC complex for multifunctionality. J Cell Biol 208:11–22PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Wang N, Tytell JD, Ingber D (2009) Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10:75–82PubMedCrossRefGoogle Scholar
  121. 121.
    Wirtz D (2009) Particle-tracking microrheology of living cells: principles and applications. Annu Rev Biophys 38:301–326PubMedCrossRefGoogle Scholar
  122. 122.
    Bell E, Ivarsson B, Merrill C (1979) Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci U S A 76:1274–1278PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Harris AK, Wild P, Stopak D (1980) Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208:177–179PubMedCrossRefGoogle Scholar
  124. 124.
    Lee J, Leonard M, Oliver T, Ishihara A, Jacobson K (1994) Traction forces generated by Locomoting Keratocytes. J Cell Biol 127:1957–1964PubMedCrossRefGoogle Scholar
  125. 125.
    Munevar S, Wang Y, Dembo M (2001) Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophys J 80:1744–1757PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Bloom RJ, George JP, Celedon A, Sun SX, Wirtz D (2008) Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multiple-particle tracking. Biophys J 95:4077–4088PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Legant WR et al (2010) Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat Methods 7:969–971PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Maskarinec SA, Franck C, Tirrell DA, Ravichandran G (2009) Quantifying cellular traction forces in three dimensions. Proc Natl Acad Sci U S A 106:22108–22113PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Fu J et al (2010) Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 7:733–736PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Tan JL et al (2003) Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci U S A 100:1484–1489PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Delvoye P, Wiliquet P, Levêque J-L, Nusgens BV, Lapière CM (1991) Measurement of mechanical forces generated by skin fibroblasts embedded in a three-dimensional collagen gel. J Invest Dermatol 97:898–902PubMedCrossRefGoogle Scholar
  132. 132.
    Vandenburgh H et al (2008) Drug-screening platform based on the contractility of tissue-engineered muscle. Muscle Nerve 37:438–447PubMedCrossRefGoogle Scholar
  133. 133.
    Zimmermann WH et al (2000) Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol Bioeng 68:106–114PubMedCrossRefGoogle Scholar
  134. 134.
    Grashoff C et al (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263–266PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Wang X et al (2013) Defining single molecular forces required to activate integrin and notch signaling. Science 340:991–994PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Blakely BL et al (2014) A DNA-based molecular probe for optically reporting cellular traction forces. Nat Methods 11:1229–1232PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Hochmuth RM (2000) Micropipette aspiration of living cells. J Biomech 33:15–22PubMedCrossRefGoogle Scholar
  138. 138.
    Yeung A, Evans E (1989) Cortical shell-liquid core model for passive flow of liquid-like spherical cells into micropipets. Biophys J 56:139–149PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Sheetz MP (2001) Cell control by membrane–cytoskeleton adhesion. Nat Rev Mol Cell Biol 2:392–396PubMedCrossRefGoogle Scholar
  140. 140.
    Dao M, Lim CT, Suresh S (2003) Mechanics of the human red blood cell deformed by optical tweezers. J Mech Phys Solids 51:2259–2280CrossRefGoogle Scholar
  141. 141.
    Mehta AD, Rief M, Spudich JA, Smith DA, Simmons RM (1999) Single-molecule biomechanics with optical methods. Science 283:1689–1695PubMedCrossRefGoogle Scholar
  142. 142.
    Felder S, Elson EL (1990) Mechanics of fibroblast locomotion: quantitative analysis of forces and motions at the leading lamellas of fibroblasts. J Cell Biol 111:2513–2526PubMedCrossRefGoogle Scholar
  143. 143.
    Athanasiou KA et al (1999) Development of the cytodetachment technique to quantify mechanical adhesiveness of the single cell. Biomaterials 20:2405–2415PubMedCrossRefGoogle Scholar
  144. 144.
    Binnig G, Quate CF, Gerber C (1986) Atomic force microscope. Phys Rev Lett 56:930–933PubMedCrossRefGoogle Scholar
  145. 145.
    Smith SB, Finzi L, Bustamante C (1992) Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258:1122–1126PubMedCrossRefGoogle Scholar
  146. 146.
    Guck J et al (2001) The optical stretcher: a novel laser tool to micromanipulate cells. Biophys J 81:767–784PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Deng L et al (2006) Fast and slow dynamics of the cytoskeleton. Nat Mater 5:636–640PubMedCrossRefGoogle Scholar
  148. 148.
    Alcaraz J et al (2003) Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys J 84:2071–2079PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Yanai M, Butler JP, Suzuki T, Sasaki H, Higuchi H (2004) Regional rheological differences in locomoting neutrophils. Am J Physiol Cell Physiol 287:603–611CrossRefGoogle Scholar
  150. 150.
    Desprat N, Richert A, Simeon J, Asnacios A (2005) Creep function of a single living cell. Biophys J 88:2224–2233PubMedCrossRefGoogle Scholar
  151. 151.
    Van Citters KM, Hoffman BD, Massiera G, Crocker JC (2006) The role of F-actin and myosin in epithelial cell rheology. Biophys J 91:3946–3956PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Crocker JC, Hoffman BD (2007) Multiple particle tracking and two-point microrheology in cells multiple particle tracking and two-point microrheology in cells multiple particle tracking and two-point microrheology in cells. Methods Cell Biol 83:141–178PubMedCrossRefGoogle Scholar
  153. 153.
    Yamada S, Wirtz D, Kuo SC (2000) Mechanics of living cells measured by laser tracking microrheology. Biophys J 78:1736–1747PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Girard KD, Kuo SC, Robinson DN (2006) Dictyostelium myosin II mechanochemistry promotes active behavior of the cortex on long time scales. Proc Natl Acad Sci U S A 103:2103–2108PubMedPubMedCentralCrossRefGoogle Scholar
  155. 155.
    Crick FHC, Hughes AFW (1950) The physical properties of cytoplasm. Exp Cell Res 1:37–80CrossRefGoogle Scholar
  156. 156.
    Fabry B, Maksym GN, Hubmayr RD, Butler JP, Fredberg JJ (1999) Implications of heterogeneous bead behavior on cell mechanical properties measured with magnetic twisting cytometry. J Magn Magn Mater 194:120–125CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Indian Institute of Science Education and Research KolkataMohanpurIndia
  2. 2.Raman Research InstituteBangaloreIndia

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