Skip to main content

Advertisement

SpringerLink
Log in

Cytoskeletal stiffness, friction, and fluidity of cancer cell lines with different metastatic potential

  • Research Paper
  • Published:
Clinical & Experimental Metastasis Aims and scope Submit manuscript

Abstract

We quantified mechanical properties of cancer cells differing in metastatic potential. These cells included normal and H-ras-transformed NIH3T3 fibroblast cells, normal and oncoprotein-overexpressing MCF10A breast cancer cells, and weakly and strongly metastatic cancer cell line pairs originating from human cancers of the skin (A375P and A375SM cells), kidney (SN12C and SN12PM6 cells), prostate (PC3M and PC3MLN4 cells), and bladder (253J and 253JB5 cells). Using magnetic twisting cytometry, cytoskeletal stiffness (g′) and internal friction (g″) were measured over a wide frequency range. The dependencies of g′ and g″ upon frequency were used to determine the power law exponent x which is a direct measure of cytoskeletal fluidity and quantifies where the cytoskeleton resides along the spectrum of solid-like (x = 1) to fluid-like (x = 2) states. Cytoskeletal fluidity x increased following transformation by H-ras oncogene expression in NIH3T3 cells, overexpression of ErbB2 and 14-3-3-ζ in MCF10A cells, and implantation and growth of PC3M and 253J cells in the prostate and bladder, respectively. Each of these perturbations that had previously been shown to enhance cancer cell motility and invasion are shown here to shift the cytoskeleton towards a more fluid-like state. In contrast, strongly metastatic A375SM and SN12PM6 cells that disseminate by lodging in the microcirculation of peripheral organs had smaller x than did their weakly metastatic cell line pairs A375P and SN12C, respectively. Thus, enhanced hematological dissemination was associated with decreased x and a shift towards a more solid-like cytoskeleton. Taken together, these results are consistent with the notion that adaptations known to enhance metastatic ability in cancer cell lines define a spectrum of fluid-like versus solid-like states, and the position of the cancer cell within this spectrum may be a determinant of cancer progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Sporn MB (1996) The war on cancer. Lancet 347:1377–1381

    Article  PubMed  CAS  Google Scholar 

  2. Chambers AF, Groom AC, MacDonald IC (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2:563–572

    Article  PubMed  CAS  Google Scholar 

  3. Gupta GP, Massagué J (2006) Cancer metastasis: building a framework. Cell 127:679–695

    Article  PubMed  CAS  Google Scholar 

  4. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70

    Article  PubMed  CAS  Google Scholar 

  5. Perou CM, Sørlie T, Eisen MB, Rijn Mvd, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge Ø, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale A-L, Brown PO, Botstein D (2000) Molecular portraits of human breast tumors. Nature 406:747–752

    Article  PubMed  CAS  Google Scholar 

  6. Futreal PA, Coin L, Marshall M, Down T, Hubbard T, Wooster R, Rhaman N, Stratton MR (2004) A census of human cancer genes. Nat Rev Cancer 4:177–183

    Article  PubMed  CAS  Google Scholar 

  7. Coussens LM, Werb Z (1996) Matrix metalloproteinases and the development of cancer. Chem Biol 3(11):895–904

    Article  PubMed  CAS  Google Scholar 

  8. Coussens LM, Fingleton B, Matrisan LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295:2387–2992

    Article  PubMed  CAS  Google Scholar 

  9. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2:161–174

    Article  PubMed  CAS  Google Scholar 

  10. Cavallaro U, Christofori G (2004) Cell adhesion and signaling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 4:118–132

    Article  PubMed  CAS  Google Scholar 

  11. Guo W, Giancotti FG (2004) Integrin signaling during tumor progression. Nat Rev Cancer 5:816–826

    Article  CAS  Google Scholar 

  12. Raz A, Geiger B (1982) Altered organization of cell-substrate contacts and membrane-associated cytoskeleton in tumor cell variants exhibiting different metastatic capabilities. Cancer Res 42:5183–5190

    PubMed  CAS  Google Scholar 

  13. 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 (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241–254

    Article  PubMed  CAS  Google Scholar 

  14. Stamenovic D, Fredberg JJ, Wang N, Butler JP, Ingber DE (1996) A microstructural approach to cytoskeletal mechanics based on tensegrity. J Theor Biol 181:125–136

    Article  PubMed  CAS  Google Scholar 

  15. Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Fredberg JJ (2001) Scaling the microrheology of living cells. Phys Rev Lett 87(14):148102

    Article  PubMed  CAS  Google Scholar 

  16. Bursac P, Lenormand G, Fabry B, Oliver M, Weitz DA, Viasnoff V, Butler JP, Fredberg JJ (2005) Cytoskeletal remodeling and slow dynamics in the living cell. Nat Mater 4:557–561

    Article  PubMed  CAS  Google Scholar 

  17. Wang N, Tolic-Nørrelykke IM, Chen J, Mijailovich SM, Butler JP, Fredberg JJ, Stamenovic D (2002) Cell prestress I. Stiffness and prestress are closely associated in adherent contractile cells. Am J Physiol Cell Physiol 282(3):C606–C616

    PubMed  CAS  Google Scholar 

  18. Laudadio RE, Millet EJ, Fabry B, An SS, Butler JP, Fredberg JJ (2005) Rat airway smooth muscle cell during actin modulation: rheology and glassy dynamics. Am J Physiol Cell Physiol 298(6):C1388–C1395

    Article  Google Scholar 

  19. Wyckoff JB, Jones JG, Condeelis JS, Segall JE (2000) A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res 60(9):2504–2511

    PubMed  CAS  Google Scholar 

  20. Shestakova EA, Wyckoff J, Jones J, Singer RH, Condeelis J (1999) Correlation of beta-actin messenger RNA localization with metastatic potential in rat adenocarcinoma cell lines. Cancer Res 59:1202–1205

    PubMed  CAS  Google Scholar 

  21. Soon L, Braet F, Condeelis J (2007) Moving in the right direction-nanoimaging in cancer cell motility and metastasis. Microsc Res Tech 70:252–257

    Article  PubMed  CAS  Google Scholar 

  22. Sahai E, Marshall CJ (2002) RHO-GTPases and cancer. Nat Rev Cancer 2:133–142

    Article  PubMed  Google Scholar 

  23. Yamazaki D, Kurisu S, Takenawa T (2005) Regulation of cancer cell motility through actin reorganization. Cancer Sci 96(7):379–386

    Article  PubMed  CAS  Google Scholar 

  24. Erickson CA (1980) The deformability of BHK cells and polyoma virus-transformed BHK cells in relation to locomotory behavior. J Cell Sci 44:187–200

    PubMed  CAS  Google Scholar 

  25. Thoumine O, Ott A (1997) Comparison of the mechanical properties of normal and transformed fibroblasts. Biorheology 34(4/5):309–326

    Article  PubMed  CAS  Google Scholar 

  26. Brooks DE (1984) The biorheology of tumor cells. Biorheology 21:85–91

    PubMed  CAS  Google Scholar 

  27. Weiss L, Asch BB, Elkin G (1991) Effects of cytoskeletal perturbation on the sensitivity of ehrlich ascites tumor cell surface membranes to mechanical trauma. INV Met 11:93–101

    CAS  Google Scholar 

  28. Ochalek T, Nordt FJ, Tullberg K, Burger MM (1988) Correlation between cell deformability and metastatic potential in B16-F1 melanoma cell variants. Cancer Res 48:5124–5128

    PubMed  CAS  Google Scholar 

  29. Wang W, Wyckoff JB, Frohlich VC, Oleynikov Y, Hüttelmaier S, Zavadil J, Cermak L, Bottinger EP, Singer RH, White JG, Segall JE, Condeelis JS (2002) Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res 62(21):6278–6288

    PubMed  CAS  Google Scholar 

  30. Egan SE, McClarty GA, Jarolm L, Wright JA, Spiro I, Hager G, Greenberg AH (1987) Expression of H-ras correlates with metastatic potential: evidence for regulation of the metastatic phenotype in 10T1/2 and NIH 3T3 cells. Mol Cell Biol 7(2):830–837

    PubMed  CAS  Google Scholar 

  31. Soule HD, Maloney TM, Wolman SR, Ward J, Peterson D, Brenz R, McGrath CM, Russo J, Pauley RJ, Jones RF, Brooks SC (1990) Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 50:6075–6086

    PubMed  CAS  Google Scholar 

  32. Debnath J, Muthuswamy SK, Brugge JS (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30:256–268

    Article  PubMed  CAS  Google Scholar 

  33. Lu J, Guo H, Treekitkarnmongkol W, Li P, Zhang J, Shi B, Ling C, Zhou X, Chen T, Chiao PJ, Feng X, Seewaldt VL, Muller WJ, Sahin A, Hung M-C, Yu D (2009) 14-3-3-ζ cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial–mesenchymal transition. Cancer Cell 16:195–207

    Article  PubMed  CAS  Google Scholar 

  34. Tambe DT, Hardin CC, Angelini TE, Rajendran K, Park CY, Serra-Picamal X, Zhou EH, Zaman MH, Butler JP, Weitz DA, Fredberg JJ, Trepat X (2011) Collective cell guidance by cooperative intercellular forces. Nat Mater 10:469–475

    Article  PubMed  CAS  Google Scholar 

  35. Elliott AY, Cleveland P, Cervenka J, Castro AE, Stein N, Hakala TR, Fraley EE (1974) Characterization of a cell line from human transitional cell cancer of the urinary tract. J Nat Cancer Inst 53(5):1341–1349

    PubMed  CAS  Google Scholar 

  36. Dinney CPN, Fishbeck R, Singh RK, Eve B, Pathak S, Brown N, Xie B, Fan D, Bucana CD, Fidler IJ, Killion JJ (1995) Isolation and characterization of metastatic variants from human transitional cell carcinoma passaged by orthotropic implantation in athymic nude mice. J Urol 154:1532–1538

    Article  PubMed  CAS  Google Scholar 

  37. Pettaway CA, Pathak S, Greene G, Ramirez E, Wilson MR, Killion JJ, Fidler IJ (1996) Selection of highly metastatic variants of different human prostatic carcinomas using orthotropic implantation in nude mice. Clin Cancer Res 2:1627–1636

    PubMed  CAS  Google Scholar 

  38. Kozlowski JM, Fidler IJ, Campbell D, Xu Z -l, Kaighn ME, Hart IR (1984) Metastatic behavior of human tumor cell lines grown in the nude mouse. Cancer Res 44:3522–3529

    PubMed  CAS  Google Scholar 

  39. Kozlowski JM, Hart IR, Fidler IJ, Hanna N (1984) A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice. J Nat Cancer Inst 72:913–917

    PubMed  CAS  Google Scholar 

  40. Naito S, Eschenbach AC v, Giavazzi R, Fidler IJ (1986) Growth and metastasis of tumor cells isolated from a human renal cell carcinoma implanted into different organs of nude mice. Cancer Res 46:4109–4115

    PubMed  CAS  Google Scholar 

  41. Naito S, Walker SM, Fidler IJ (1989) In vivo selection of human renal cell carcinoma cells with high metastatic potential in nude mice. Clin Exp Metastasis 7(4):381–389

    Article  PubMed  CAS  Google Scholar 

  42. Fabry B, Maksym GN, Shore SA, Moore PE, Reynold J, Panettieri A, Butler JP, Fredberg JJ (2001) Time course and heterogeneity of contractile responses in cultured human airway smooth muscle cells. J Appl Physiol 91:986–994

    PubMed  CAS  Google Scholar 

  43. Wang N, Butler JP, Ingber DE (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260:1124–1127

    Article  PubMed  CAS  Google Scholar 

  44. Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Taback NA, Millet EJ, Fredberg JJ (2003) Time scale and other invariants of integrative mechanical behavior in living cells. Phys Rev E 68(041914):041914

    Article  Google Scholar 

  45. Puig-de-Morales-Marinkovic M, Turner KT, Butler JP, Fredberg JJ, Suresh S (2007) Viscoelasticity of the human red blood cell. Am J Cell Physiol 293:C597–C605

    Article  CAS  Google Scholar 

  46. Valberg PA, Butler JP (1987) Magnetic particle motions within living cells. Physical theory and techniques. Biophys J 52:537–550

    Article  PubMed  CAS  Google Scholar 

  47. Lenormand G, Fredberg JJ (2006) Deformability, dynamics, and remodeling of cytoskeleton of the adherent living cell. Biorheology 43(1):1–30

    PubMed  Google Scholar 

  48. Sollich P (1998) Rheological constitutive equation for a model of soft glassy materials. Phys Rev E 58(1):738–759

    Article  CAS  Google Scholar 

  49. Puig-de-Morales M, Millet E, Fabry B, Navajas D, Wang N, Butler JP, Fredberg JJ (2004) Cytoskeletal mechanics in the adherent human airway smooth muscle cells: probe specificity and scaling of protein–protein dynamics. Am J Physiol Cell Physiol 287(3):C643–C654

    Article  PubMed  CAS  Google Scholar 

  50. Weiss NA, Hassett MJ (1991) Introductory statistics. Addison-Wesley, Reading

    Google Scholar 

  51. Lenormand G, Millet E, Fabry B, Butler JP, Fredberg JJ (2004) Linearity and time-scale invariance of the creep function in living cells. J R Soc Interface 1(1):91–97

    Article  PubMed  CAS  Google Scholar 

  52. Fielding SM, Sollich P, Cates ME (2000) Aging and rheology in soft materials. J Rheol 44(2):323–369

    Article  CAS  Google Scholar 

  53. Coughlin MF, Puig-de-Morlaes M, Bursac P, Mellema M, Millet E, Fredberg JJ (2006) Filamin-A and rheological properties of cultured melanoma cells. Biophys J 90(6):2199–2205

    Article  PubMed  CAS  Google Scholar 

  54. Remmerbach TW, Wottawah F, Dietrich J, Lincoln B, Wittekind C, Guck J (2009) Oral cancer diagnosis by mechanical phenotyping. Cancer Res 69(5):1728–1732

    Article  PubMed  CAS  Google Scholar 

  55. Darling EM, Topel M, Zauscher S, Vail TP, Guilak F (2008) Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J Biomech 41:454–464

    Article  PubMed  Google Scholar 

  56. Cross SE, Jin Y, Rao J, Gimzewski JK (2007) Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol 2:780–783

    Article  PubMed  CAS  Google Scholar 

  57. Rosenbluth MJ, Lam WA, Fletcher DA (2006) Force microscopy of nonadherent cells: a comparison of leukemia cell deformability. Biophys J 90:2994–3003

    Article  PubMed  CAS  Google Scholar 

  58. Weiss L (1992) Biomechanical interactions of cancer cells with the microvasculature during hematogenous metastasis. Cancer Metastasis Rev 11:227–235

    Article  PubMed  CAS  Google Scholar 

  59. Worthen GS, Schwab B III, Elson EL, Downey GP (1989) Mechanics of stimulated neutrophils: cell stiffening induces retention in capillaries. Science 245:183–186

    Article  PubMed  CAS  Google Scholar 

  60. Petersen NO, McConnaughey WB, Elson EL (1981) Investigations of structural determinants of cell shape. Commun Mol Cell Biophys 1(3):135–147

    Google Scholar 

  61. Desgrosellier JS, Cheresh DA (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 10:9–22

    Article  PubMed  CAS  Google Scholar 

  62. Varner JA, Cheresh DA (1996) Integrins and cancer. Curr Opin Cell Biol 8:724–730

    Article  PubMed  CAS  Google Scholar 

  63. Darling EM, Zauscher S, Block JA, Guilak F (2007) A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential? Biophys J 92:1784–1791

    Article  PubMed  CAS  Google Scholar 

  64. Li Y, Schnekenburger J, Duits MGH (2009) Intracellular particle tracking as a tool for tumor cell characterization. J Biomed Opt 14(6):064005

    Article  PubMed  Google Scholar 

  65. Docheva D, Padula D, Popov C, Mutschler W, Clausen-Schaumann H, Schieker M (2008) Researching into the cellular shape, volume and elasticity of mesenchymal stem cells, osteoblasts and osteosarcoma cells by atomic force microscopy. J Cell Mol Med 12(2):537–552

    Article  PubMed  Google Scholar 

  66. Shim S, Kim MG, Jo K, Kang YS, Lee B, Yang S, Shin S-M, Lee J-H (2010) Dynamic characterization of human breast cancer cells using a piezoresistive microcantilever. J Biomech Eng 132:104501

    Article  PubMed  Google Scholar 

  67. Guck J, Schinkinger S, Lincoln B, Wottawah F, Ebert S, Romeyke M, Lenz D, Erickson HM, Ananthakrishnan R, Mitchell D, Käs J, Ulvick S, Bilby C (2005) Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys J 88(5):3689–3698

    Article  PubMed  CAS  Google Scholar 

  68. Lincoln B, Erickson HM, Schinkinger S, Wottawah F, Mitchell D, Ulvick S, Bilby C, Guck J (2004) Deformability-based flow cytometry. Cytometry A 59A:203–209

    Article  Google Scholar 

  69. Sato H, Suzuki M (1976) Deformability and viability of tumor cells by transcapillary passage, with reference to organ affinity of metastasis in cancer. In: Weiss L (ed) Functional aspects of metastasis. North-Holland, Amsterdam, pp 311–317

    Google Scholar 

  70. Sato H, Khato J, Sato T, Suzuki M (1977) Deformability and filterability of tumor cells through “Nucleopore” filter, with reference to viability and metastatic spread. GANN Monogr Cancer Res 20:3–13

    Google Scholar 

  71. Ward KA, Li W-I, Zimmer S, Davis T (1991) Viscoelastic properties of transformed cells: role in tumor cell progression and metastasis formation. Biorheology 28(3–4):301–313

    PubMed  CAS  Google Scholar 

  72. Bao N, Zhan Y, Lu C (2008) Microfluidic electroporative flow cytometry for studying single-cell biomechanics. Anal Chem 80:7714–7719

    Article  PubMed  CAS  Google Scholar 

  73. Baker EL, Lu J, Yu D, Bonnecaze RT, Zaman MH (2010) Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys J 99:2048–2057

    Article  PubMed  CAS  Google Scholar 

  74. Li QS, Lee GYH, Ong CN, Lim CT (2008) AFM indentation study of breast cancer cells. Biochem Biophys Res Commun 374:609–613

    Article  PubMed  CAS  Google Scholar 

  75. Guido I, Jaeger MS, Duschl C (2011) Dielectrophoretic stretching of cells allows for characterization of their mechanical properties. Eur Biophys J 40:281–288

    Article  PubMed  Google Scholar 

  76. Elsässer H-P, Lehr U, Agricola B, Kern HF (1992) Establishment and characterisation of two cell lines with different grade of differentiation derived from one primary human pancreatic adenocarcinoma. Virchows Arch B Cell Pathol 61:295–306

    Article  Google Scholar 

  77. Cross SE, Jin Y-S, Tondre J, Wong R, Rao JY, Gimzewski JK (2008) AFM-based analysis of human metastatic cancer cells. Nanotechnology 19:384003

    Article  PubMed  Google Scholar 

  78. Oh WK, Hurwitz M, D’Amico AV, Richie JP, Kantoff PW (2003) Neoplasms of the prostate. In: Kufe DW (ed) Cancer medicine, 6th edn. Decker, Hamilton, pp 1707–1740

    Google Scholar 

  79. Anderson KW, Li W-I, Cezeaux J, Zimmer S (1992) In vitro studies of deformation and adhesion properties of transformed cells. Cell Biophys 18(2):81–97

    Google Scholar 

  80. Lekka M, Laidler P, Gil D, Lekki J, Stachura Z, Hrynkiewicz AZ (1999) Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Eur Biophys J 28:312–316

    Article  PubMed  CAS  Google Scholar 

  81. Lekka M, Laidler P, Ignacak J, Labedz M, Lekki J, Struszczyk H, Stachura Z, Hrynkiewicz AZ (2001) The effect of chitosan on stiffness and glycolytic activity of human bladder cells. Biochim Biophys Acta 1540:127–136

    Article  PubMed  CAS  Google Scholar 

  82. Park S, Koch D, Cardenas R, Käs J, Shih CK (2005) Cell motility and local viscoelasticity of fibroblasts. Biophys J 89:4330–4342

    Article  PubMed  CAS  Google Scholar 

  83. Reed J, Frank M, Troke JJ, Schmit J, Han S, Teitell MA, Gimzewski JK (2008) High throughput cell nanomechanics with mechanical imaging interferometry. Nanotechnology 19:235101

    Article  PubMed  Google Scholar 

  84. Wottawah F, Schinkinger S, Lincoln B, Anathakrishnan R, Romeyke M, Guck J, Käs J (2005) Optical rheology of biological cells. Phys Rev Lett 94:098103

    Article  PubMed  Google Scholar 

  85. Zhang G, Long M, Wu Z-Z, Yu W-Q (2002) Mechanical properties of hepatocellular carcinoma cells. World J Gastroenterol 8(2):243–246

    PubMed  Google Scholar 

  86. Wang N, Ingber DE (1994) Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys J 66(June):2181–2189

    Article  PubMed  CAS  Google Scholar 

  87. Coughlin MF, Stamenovic D (1998) A tensegrity model of the cytoskeleton in spread and round cells. J Biomech Eng 120(6):770–777

    Article  PubMed  CAS  Google Scholar 

  88. Balland M, Desprat N, Icard D, Féréol S, Asnacios A, Browaeys J, Hénon S, Gallet F (2006) Power laws in microrheology experiments on living cells: comparative analysis and modeling. Phys Rev E 74:021911

    Article  Google Scholar 

  89. Trepat X, Deng L, An SS, Navajas D, Tschumperlin DJ, Gerthoffer WT, Butler JP, Fredberg JJ (2007) Universal physical responses to stretch in the livingcell. Nature 447:592–596

    Article  PubMed  CAS  Google Scholar 

  90. Fabry B, Fredberg JJ (2003) Remodeling of the airway smooth muscle cell: are we built of glass. Respir Physiol Neurobiol 137(2–3):109–124

    Article  PubMed  Google Scholar 

  91. Sollich P, Lequeux F, Hébraud P, Cates ME (1997) Rheology of soft glassy materials. Phys Rev Lett 78(10):2020–2023

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Transfected MCF-10A cell lines were a kind gift from Dr. Muhammad Zaman (Boston University, Boston, MA).The cancer cell lines 253J, 253JB5, A375P, A375SM, PC3M, PC3MLN4, SN12C, and SN12PM6 were kindly provided by Dr. Isaiah J. Fidler (M.D. Anderson Cancer Center, Houston, TX). G.L. was supported by the Parker B. Francis Foundation. D.R.B. was funded by NCI CA118732 and CA155728. J.J.F. was funded by R01HL107561, R01HL102373, and R01EY019696.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard School of Public Health, 665 Huntington Avenue, Boston, MA, 02115, USA

    Mark F. Coughlin, Guillaume Lenormand, Marina Marinkovic & Jeffrey J. Fredberg

  2. Vascular Biology Program, Boston Children’s Hospital, Department of Surgery, Harvard Medical School, 300 Longwood Avenue, Boston, MA, 02115, USA

    Diane R. Bielenberg & Bruce R. Zetter

  3. ArQule, 19 Presidental Way, Woburn, MA, 01801, USA

    Carol G. Waghorne

Authors
  1. Mark F. Coughlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diane R. Bielenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guillaume Lenormand
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marina Marinkovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carol G. Waghorne
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bruce R. Zetter
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jeffrey J. Fredberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark F. Coughlin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Coughlin, M.F., Bielenberg, D.R., Lenormand, G. et al. Cytoskeletal stiffness, friction, and fluidity of cancer cell lines with different metastatic potential. Clin Exp Metastasis 30, 237–250 (2013). https://doi.org/10.1007/s10585-012-9531-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10585-012-9531-z

Keywords

Search

Navigation