Biomechanical profile of cancer stem-like/tumor-initiating cells derived from a progressive ovarian cancer model

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 10, Issue 5, 2014, Pages e1013-e1019

  Babahosseini, Hesam ^a   Ketene, Alperen N ^a   Schmelz, Eva M ^b   Roberts, Paul C ^c   Agah, Masoud ^a  

^a Virginia Polytechnic Institute and State University   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

Author keywords

Atomic force microscope; Cancer chemotherapy; Cancer stem like tumor initiating cells; Cell biomechanics; Cellular differentiation

Indexed keywords

ATOMIC FORCE MICROSCOPY; CELL CULTURE; CHEMOTHERAPY; DISEASES; ELASTIC MODULI; STEM CELLS;

ANTI-CANCER AGENTS; CANCER CHEMOTHERAPY; CANCER DETECTION; CANCER STEM CELLS; CELL BIOMECHANICS; CELLULAR DIFFERENTIATION; ELASTIC MODULUS MEASUREMENTS; OVARIAN CANCERS;

BIOMECHANICS;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CANCER DIAGNOSIS; CANCER GROWTH; CANCER STEM CELL; CELL DIFFERENTIATION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; FEMALE; HISTOGRAM; MOUSE; NONHUMAN; OVARY CANCER; PHENOTYPE; RIGIDITY; ANIMAL; CELL TRANSFORMATION; CYTOLOGY; DISEASE COURSE; METABOLISM; OVARY TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

MURINAE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; FEMALE; MICE; MICROSCOPY, ATOMIC FORCE; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS;

EID: 84903532893     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2013.12.009     Document Type: Article

References (42)

1. Nowell P.C. The clonal evolution of tumor cell populations. Science 1976, 194(4260):23-28.
2. Teitell M.A., Kalim S., Schmitt J., Reed J. Biomechanics of single cells and cell populations. Nanodiamonds: Applications in Biology and Nanoscale Medicine 2010, 235-247. D. Ho (Ed.).
3. Park C.H., Bergsagel D.E., Mcculloch E.A. Mouse myeloma tumor stem cells: a primary cell culture assay. J Natl Cancer Inst 1971, 46:411-422.
4. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
5. Suresh S. Biomechanics and biophysics of cancer cells. Acta Biomater 2007, 3:413-438.
6. Roberts P.C., Motillo E., Baxa A.C., Heng H.H.Q., Doyon-Reale N., Gregoire L., et al. Sequential molecular and cellular events during neoplastic progression: a mouse syngeneic ovarian cancer model. Neoplasia 2005, 7:944-956.
7. Creekmore A.L., Silkworth W.T., Cimini D., Jensen R.V., Roberts P.C., Schmelz E.M. Changes in gene expression and cellular architecture in an ovarian cancer progression model. PLoS ONE 2011, 6(3):e17676.
8. Ketene A.N., Schmelz E.M., Roberts P.C., Agah M. The effects of cancer progression on the viscoelasticity of ovarian cell cytoskeleton structures. Nanomedicine: Nanotechnology, Biology, and Medicine 2011, 8:93-102.
9. Ketene A.N., Roberts P.C., Shea A.A., Schmelz E.M., Agah M. Actin filaments play a primary role for structural integrity and viscoelastic response in cells. Integr Biol 2012, 4:540-549.
10. Nikkhah M., Strobl J., De Vita R., Agah M. The cytoskeletal organization of breast carcinoma and fibroblast cells inside three dimensional (3-D) isotropic silicon microstructures. Biomaterials 2010, 31(16):1-10.
11. Nikkhah M., Strobel J.S., Schmelz E.M., Agah M. Evaluation of the influence of growth medium composition on cell elasticity. J Biomech 2011, 44(4):762-766.
12. Faria E.C., Ma N., Gazi E., Gardner P., Brown M., Clarke N.W., et al. Measurement of elastic properties of prostate cancer cells using AFM. Analyst 2008, 133(11):1498-1500.
13. Lekka M., Laidler P., Gil D., Lekki J., Stachura Z., Hrynkiewicsm A.Z. Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Biophysics Journal 1999, 28:312-316.
14. Weder G., Hendriks-Balk M.C., Smajda R., Rimoldi D., Liley M., Heinzelmann H. Increased plasticity of the stiffness of melanoma cells correlates with their acquisition of metastatic properties. Nanotechnol Biol Med 2014, 10(1):141-148.
15. 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(10):e46609.
16. Pajerowski J.D., Dahl K.N., Zhong F.L., Sammak P.J., Discher D.E. Physical plasticity of the nucleus in stem cell differentiation. PNAS 2007, 104(40):15619-15624.
17. Chowdhury F., Na S., Li D., Poh Y.C., Tanaka T.S., Wang F., et al. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat Mater 2010, 9(1):82-88.
18. Titushkin I., Cho M. Modulation of cellular mechanics during osteogenic differentiation of human mesenchymal stem cells. Biophys Journal 2007, 93(10):3693-3702.
19. Zhang W., Kai K., Choi D.S., Iwamoto T., Nguyen Y.H., Wong H., et al. Microfluidics separation reveals the stem-cell-like deformability of tumor-initiating cells. PNAS 2012, 109(46):18707-18712.
20. Creekmore A.L., Heffron C.L., Brayfield B., Roberts P.C., Schmelz E.M. Regulation of cytoskeleton organization by sphingosine in a mouse cell model of progressive ovarian cancer. Biomolecules 2013, 3:386-407.
21. Bodine P.V.N., Henderson R.A., Green J., Aronow M., Owen T., Stein G.S., et al. Estrogen receptor-alfa is developmentally regulated during osteoblast differentiation and contributes to selective responsiveness of gene expression. Endocrinology 1998, 139(4):2048-2057.
22. Ben-Ze'ev A. The role of changes in cell shape and contacts in the regulation of cytoskeleton expression during differentiation. J Cell Sci Suppl 1987, 8:298-312.
23. Rodriguez Fernandez J.L., Ben-Ze'ev A. Regulation of fibronectin, integrin and cytoskeleton expression in differentiating adipocytes: inhibition by extracellular matrix and polylysine. Differentiation 1989, 42(2):65-74.
24. Sell S. Cellular origin of cancer: dedifferentiation or stem cell maturation arrest?. Environ Health Perspect 1993, 101(Suppl. 5):15-26.
25. Gault C.R., Obeid L.M., Hannun Y.A. An overview of sphingolipid metabolism: from synthesis to breakdown. Adv Exp Med Biol 2010, 688:1-23.
26. Babahosseini H., Roberts P.C., Schmelz E.M., Agah M. Bioactive sphingolipid metabolites modulate ovarian cell structural mechanics in the progression of Cancer. Integr Biol 2013, 5:1385-1392.
27. Hertz H. On the contact of elastic solids. J Reine Angew Math 1881, 92:156-171.
28. Sneddon I.N. The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile. Int J Eng Sci 1965, 3:47-57.
29. Darling E.M., Zauscher S., Block J.M., 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.
30. Cross S.E., Jin Y., Rao J., Gimzewski J.K. Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol 2007, 2:780-783.
31. Guo S.L., Akhremitchev B.B. Packing density and structural heterogeneity of insulin fibrils by AFM nanoindentation. J Biomacromolecules 2006, 7:1630-1636.
32. Carl P., Schillers H. Elasticity measurement of living cells with an atomic force microscope: data acquisition and processing. Pflugers Arch-Eur J Physiol 2008, 457:551-559.
33. Rico F., Roca-Cusachs P., Gavara N., Farre R., Rotger M., Navajas D. Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. J Phys Rev E 2005, 72:1-10.
34. Sen S., Subramanian S., Discher D.E. Indentation and adhesive probing of a cell membrane with AFM: theoretical model and experiments. Biophys J 2005, 89:3203-3213.
35. Cohen C.A., Shea A.A., Heffron C.L., Schmelz E.M., Roberts P.C. Intra-abdominal fat depots represent distinct immunomodulatory microenvironments. PLoS One 2013, 8(6):e66477.
36. Cohen C.A., Shea A.A., Heffron C.L., Schmelz E.M., Roberts P.C. Parity-associated protection against ovarian cancer metastasis in the omental fat band. Cancer Prev Res 2013, 6:1182-1193.
37. Rappa G., Mercapide J., Anzanello F., Prasmickaite L., Xi Y., Ju J., et al. Growth of cancer cell lines under stem cell-like conditions has the potential to unveil therapeutic targets. Exp Cell Res 2008, 314:2110-2122.
38. Feng D., Peng C., Li C., Zhou Y.I., Li M., Ling B., et al. Identification and characterization of cancer stem-like cells from primary carcinoma of the cervix uteri. Oncol Rep 2009, 22:1129-1134.
39. Zhu C., Bao G., Wang N. Cell mechanics: mechanical response, cell adhesion, and molecular deformation. Annu Rev Biomed Eng 2000, 2:189-226.
40. Adamo A., Sharei A., Adamo L., Lee B.K., Mao S., Jensen K.F. Microfluidics-based assessment of cell deformability. Anal Chem 2012, 84:6438-6443.
41. Zheng Y., Shojaei-Baghini E., Azad A., Wang C., Sun Y. High-throughput biophysical measurement of human red blood cells. Lab Chip 2012, 12:2560-2567.
42. Hou H.W., Li Q.S., Lee G.Y.H., Kumar A.P., Ong C.N., Lim C.T. Deformability study of breast cancer cells using microfluidics. Biomed Microdevices 2009, 11:557-564.