Mechanical properties of fibroblasts depend on level of cancer transformation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 5, 2014, Pages 1013-1019

  Efremov, Yu M ^a   Lomakina, M E ^b   Bagrov, D V ^a   Makhnovskiy, P I ^a   Alexandrova, A Y ^b   Kirpichnikov, M P ^a   Shaitan, K V ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b N N BLOKHIN RUSSIAN CANCER RESEARCH CENTER   (Russian Federation)

Author keywords

AFM; Fibroblast; Force spectroscopy; Transformed cell; Young's modulus

Indexed keywords

AFM; FIBROBLAST; FORCE SPECTROSCOPY; TRANSFORMED CELL; YOUNG'S MODULUS;

CELL TRANSFORMATION, NEOPLASTIC; FIBROBLASTS; FOCAL ADHESIONS; HUMANS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE;

EID: 84894496770     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.01.032     Document Type: Article

References (51)

1. Kumar S., Weaver V.M. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 2009, 28:113-127.
2. Katira P., Zaman M.H., Bonnecaze R.T. How changes in cell mechanical properties induce cancerous behavior. Phys. Rev. Lett. 2012, 108:028103.
3. Makale M. Cellular mechanobiology and cancer metastasis. Birth Defects Res. C 2007, 81:329-343.
4. Lekka M., Pogoda K., Gostek J., Klymenko O., Prauzner-Bechcicki S., Wiltowska-Zuber J., Jaczewska J., Lekki J., Stachura Z. Cancer cell recognition-mechanical phenotype. Micron 2012, 43:1259-1266.
5. Xu W., Mezencev R., Kim B., Wang L., McDonald J., Sulchek T. Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLoS One 2012, 7:e46609.
6. Swaminathan V., Mythreye K., O'Brien E.T., Berchuck A., Blobe G.C., Superfine R. Mechanical stiffness grades metastatic potential in patient tumor cells and in cancer cell lines. Cancer Res. 2011, 71:5075-5080.
7. Ketene A.N., Schmelz E.M., Roberts P.C., Agah M. The effects of cancer progression on the viscoelasticity of ovarian cell cytoskeleton structures. Nanomed. Nanotechnol. Biol. Med. 2011, 8:93-102.
8. Darling E.M., Zauscher S., Block J.a, Guilak F. A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential?. Biophys. J. 2007, 92:1784-1791.
9. Bastatas L., Martinez-Marin D., Matthews J., Hashem J., Lee Y.J., Sennoune S., Filleur S., Martinez-Zaguilan R., Park S. AFM nano-mechanics and calcium dynamics of prostate cancer cells with distinct metastatic potential. Biochim. Biophys. Acta 2012, 1820:1111-1120.
10. Faria E.C., Ma N., Gazi E., Gardner P., Brown M., Clarke N.W., Snook R.D. Measurement of elastic properties of prostate cancer cells using AFM. Analyst 2008, 133:1498-1500.
11. Zhang G., Long M., Wu Z.-Z., Yu W.-Q. Mechanical properties of hepatocellular carcinoma cells. World J. Gastroenterol. 2002, 8:243-246.
12. Radmacher M. Measuring the elastic properties of living cells by the atomic force microscope. Methods Cell Biol. 2002, 68:67-90.
13. Fletcher D.a, Mullins R.D. Cell mechanics and the cytoskeleton. Nature 2010, 463:485-492.
14. Li Q.S., Lee G.Y.H., Ong C.N., Lim C.T. AFM indentation study of breast cancer cells. Biochem. Biophys. Res. Commun. 2008, 374:609-613.
15. Vasiliev J.M. Cytoskeletal mechanisms responsible for invasive migration of neoplastic cells. Int. J. Dev. Biol. 2004, 48:425-440.
16. Olson M.F., Sahai E. The actin cytoskeleton in cancer cell motility. Clin. Exp. Metastasis 2009, 26:273-287.
17. Mehlen P., Puisieux A. Metastasis: a question of life or death. Nat. Rev. Cancer 2006, 6:449-458.
18. Rotsch C., Radmacher M. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys. J. 2000, 78:520-535.
19. Park S., Koch D., Cardenas R., Käs J., Shih C.K. Cell motility and local viscoelasticity of fibroblasts. Biophys. J. 2005, 89:4330-4342.
20. Shutova M.S., Alexandrova A.Y. Normal and transformed fibroblast spreading: role of microfilament polymerization and actin-myosin contractility. Cell Tissue Biol. 2010, 4:25-35.
21. Hoffman B.D., Crocker J.C. Cell mechanics: dissecting the physical responses of cells to force. Annu. Rev. Biomed. Eng. 2009, 11:259-288.
22. Kasza K.E., Rowat A.C., Liu J., Angelini T.E., Brangwynne C.P., Koenderink G.H., Weitz D.A. The cell as a material. Curr. Opin. Cell Biol. 2007, 19:101-107.
23. Lekka M., Gil D., Pogoda K., Dulińska-Litewka J., Jach R., Gostek J., Klymenko O., Prauzner-Bechcicki S., Stachura Z., Wiltowska-Zuber J., Okoń K., Laidler P. Cancer cell detection in tissue sections using AFM. Arch. Biochem. Biophys. 2011, 518:151-156.
24. Efremov Y.M., Bagrov D.V., Dubrovin E.V., Shaitan K.V., Yaminskii I.V. Atomic force microscopy of animal cells: advances and prospects. Biophysics 2011, 56:257-267.
25. Kasas S., Longo G., Dietler G. Mechanical properties of biological specimens explored by atomic force microscopy. J. Phys. D. Appl. Phys. 2013, 46:133001.
26. Harvey D.M., Levine A.J. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 1991, 5:2375-2385.
27. Lomakina M.E., Alexandrova A.Y. Analysis of changes induced by oncogene N-RAS expression in pattern and distribution of pseudopodial activity of fibroblasts. Russ. J. Dev. Biol. 2009, 40:222-231.
28. Huschtscha L.I., Holliday R. Limited and unlimited growth of SV40-transformed cells from human diploid MRC-5 fibroblasts. J. Cell Sci. 1983, 63:77-99.
29. Rasheed S., Nelson-Rees W.A., Toth E.M., Arnstein P., Gardner M.B. Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 1974, 33:1027-1033.
30. Efremov Y.M., Dokrunova A.A., Bagrov D.V., Kudryashova K.S., Sokolova O.S., Shaitan K.V. The effects of confluency on cell mechanical properties. J. Biomech. 2013, 46:1081-1087.
31. Lu Y.B., Franze K., Seifert G., Steinhauser C., Kirchhoff F., Wolburg H., Guck J., Janmey P., Wei E.Q., Kas J., Reichenbach A. Viscoelastic properties of individual glial cells and neurons in the CNS. Proc. Natl. Acad. Sci. 2006, 103:17759-17764.
32. Alexandrova A.Y., Dugina V.B., Paterson H., Bershadsky A.D., Vasiliev J.M. Motility of intracellular particles in rat fibroblasts is greatly enhanced by phorbol ester and by over-expression of normal p21N-ras. Cell Motil. Cytoskeleton 1993, 25:254-266.
33. Minina S.A., Aleksandrova A.Y., Vasil'ev Y.M. Changes in the cell shape and actin cytoskeleton during the Ras oncogene-induced transformation: a possible role of Rho kinase. Dokl. Biol. Sci. 2003, 388:83-85.
34. Dimitriadis E.K., Horkay F., Maresca J., Kachar B., Chadwick R.S. Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 2002, 82:2798-2810.
35. Kuznetsova T.G., Starodubtseva M.N., Yegorenkov N.I., Chizhik S.A., Zhdanov R.I. Atomic force microscopy probing of cell elasticity. Micron 2007, 38:824-833.
36. Cross S.E., Jin Y.S., Rao J., Gimzewski J.K. Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2007, 2:780-783.
37. Hiratsuka S., Mizutani Y., Tsuchiya M., Kawahara K., Tokumoto H., Okajima T. The number distribution of complex shear modulus of single cells measured by atomic force microscopy. Ultramicroscopy 2009, 109:937-941.
38. Mizutani Y., Tsuchiya M., Hiratsuka S., Kawahara K., Tokumoto H., Okajima T. Elasticity of living cells on a microarray during the early stages of adhesion measured by atomic force microscopy. Jpn. J. Appl. Phys. 2008, 47:6177-6180.
39. Alenghat F.J., Fabry B., Tsai K.Y., Goldmann W.H., Ingber D.E. Analysis of cell mechanics in single vinculin-deficient cells using a magnetic tweezer. Biochem. Biophys. Res. Commun. 2000, 277:93-99.
40. Fabry B., Maksym G.N., Shore S.A., Moore P.E., Panettieri R.A., Butler J.P., Fredberg J.J. Selected contribution: time course and heterogeneity of contractile responses in cultured human airway smooth muscle cells. J. Appl. Physiol. 2001, 91:986-994.
41. Hoffman B.D., Massiera G., Van Citters K.M., Crocker J.C. The consensus mechanics of cultured mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10259-10264.
42. Guck J., Schinkinger S., Lincoln B., Wottawah F., Ebert S., Romeyke M., Lenz D., Erickson H.M., Ananthakrishnan R., Mitchell D., Käs J., Ulvick S., Bilby C. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 2005, 88:3689-3698.
43. Barbacid M. ras Genes. Annu. Rev. Biochem. 1987, 56:779-827.
44. Moon A., Kim M.S., Kim T.G., Kim S.H., Kim H.E., Chen Y.Q., Kim H.R. H-ras, but not N-ras, induces an invasive phenotype in human breast epithelial cells: a role for MMP-2 in the h-ras-induced invasive phenotype. Int. J. Cancer 2000, 85:176-181.
45. Dayaram T., Marriott S. Effect of transforming viruses on molecular mechanisms associated with cancer. J. Cell. Physiol. 2008, 216:309-314.
46. Benedict W., Weissman B., Mark C., Stanbridge E. Tumorigenicity of human HT1080 fibrosarcoma X normal fibroblast hybrids: chromosome dosage dependency. Cancer Res. 1984, 44:3471-3479.
47. Cha H.J., Bae S.K., Lee H.Y., Lee O.H., Sato H., Seiki M., Park B.C., Kim K.W. Anti-invasive activity of ursolic acid correlates with the reduced expression of matrix metalloproteinase-9 (MMP-9) in HT1080 human fibrosarcoma cells. Cancer Res. 1996, 56:2281-2284.
48. Plodinec M., Loparic M., Monnier C.A., Obermann E.C., Zanetti-Dallenbach R., Oertle P., Hyotyla J.T., Aebi U., Bentires-Alj M., Lim R.Y.H., Schoenenberger C.A. The nanomechanical signature of breast cancer. Nat. Nanotechnol. 2012, 7:757-765.
49. Sokolov I. Atomic force microscopy in cancer cell research. Cancer Nanotechnology 2007, 1-17. American Scientific Publishers, Valencia. H. Singh Nalwa, T. Webster (Eds.).
50. Fritsch A., Höckel M., Kiessling T., Nnetu K.D., Wetzel F., Zink M., Kas J.A. Are biomechanical changes necessary for tumour progression?. Nat. Phys. 2010, 6:730-732.
51. Wirtz D., Konstantopoulos K., Searson P.C. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer 2011, 11:512-522.