The Roles of Cellular Nanomechanics in Cancer

Medicinal Research Reviews

Volumn 35, Issue 1, 2015, Pages 198-223

  Yallapu, Murali M ^a   Katti, Kalpana S ^b   Katti, Dinesh R ^b   Mishra, Sanjay R ^c   Khan, Sheema ^a   Jaggi, Meena ^a   Chauhan, Subhash C ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b North Dakota State University   (United States)

^c University of Memphis   (United States)

Author keywords

Anticancer drugs; Atomic force microscopy; Cancer cells; Cancer therapeutics; Cellular elasticity; Cellular mechanics; Nanomechanical properties

Indexed keywords

ANTINEOPLASTIC AGENT;

ARTICLE; ATOMIC FORCE MICROSCOPY; CANCER CELL; CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER GROWTH; CANCER THERAPY; CANCER TISSUE; CELL ADHESION; CELL FUNCTION; CELL INTERACTION; CELL MEMBRANE; CELL PROLIFERATION; CELL SURFACE; CELL ULTRASTRUCTURE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR MECHANICS; YOUNG MODULUS; NANOTECHNOLOGY; NEOPLASMS; PATHOLOGY; VALIDATION STUDY;

HUMANS; MICROSCOPY, ATOMIC FORCE; NANOTECHNOLOGY; NEOPLASMS;

EID: 84915778584     PISSN: 01986325     EISSN: 10981128     Source Type: Journal    
DOI: 10.1002/med.21329     Document Type: Article

References (126)

1. http://www.wcrf.org/cancer_statistics/world_cancer_statistics.php.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63(1):11-30.
3. Lekka M, Laidler P, Gil D, Lekki J, Stachura Z, Hrynkiewicz AZ. Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Eur Biophys J 1999;28(4):312-316.
4. Guck J, Schinkinger S, Lincoln B, Wottawah F, Ebert S, Romeyke M, Lenz D, Erickson H, 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(5):3689-3698.
5. Lal R, Arnsdorf MF. Multidimensional atomic force microscopy for drug discovery: A versatile tool for defining targets, designing therapeutics and monitoring their efficacy. Life Sci 2010;86(15-16):545-562.
6. Muller DJ, Dufrene YF. Atomic force microscopy: A nanoscopic window on the cell surface. Trends Cell Biol 2011;21(8):461-469.
7. Schuh CA. Nanoindentation studies of materials. Mater Today 2006;9(5):32-40.
8. Wang J, Wan Z, Liu W, Li L, Ren L, Wang X, Sun P, Zhao H, Tu Q, Zhang Z, Song N, Zhang L. Atomic force microscope study of tumor cell membranes following treatment with anti-cancer drugs. Biosens Bioelectron 2009;25(4):721-727.
9. Pillet F, Chopinet L, Formosa C, Dague E. Atomic force microscopy and pharmacology: From microbiology to cancerology. Biochim Biophys Acta 2014;1840(3):1028-1050.
10. Babahosseini H, Ketene AN, Schmelz EM, Roberts PC, Agah M. Biomechanical profile of cancer stem-like/tumor initiating cells derived from a progressive ovarian cancer model. Nanomedicine 2014;10(5):1013-1019.
11. Yang R, Xi N, Fung CK, Seiffert-Sinha K, Lai KW, Sinha AA. The emergence of AFM applications to cell biology: How new technologies are facilitating investigation of human cells in health and disease at the nanoscale. J Nanosci Lett 2011;1(2):87-101.
12. Edwardson JM, Henderson RM. Atomic force microscopy and drug discovery. Drug Discov Today 2004;9(2):64-71.
13. Kuznetsova TG, Starodubtseva MN, Yegorenkov NI, Chizhik SA, Zhdanov RI. Atomic force microscopy probing of cell elasticity. Micron 2007;38(8):824-833.
14. Chen PY, Lin AY, Lin YS, Seki Y, Stokes AG, Peyras J, Olevsky EA, Meyers MA, McKittrick J. Structure and mechanical properties of selected biological materials. J Mech Behav Biomed Mater 2008;1(3):208-226.
15. Chen PY, McKittrick J, Meyers MA. Biological materials: Functional adaptations and bioinspired designs. Prog Mater Sci 2012;57(8):1492-1704.
16. Su HN, Chen ZH, Song XY, Chen XL, Shi M, Zhou BC, Zhao X, Zhang YZ. Antimicrobial peptide trichokonin VI-induced alterations in the morphological and nanomechanical properties of Bacillus subtilis. PLoS One 2012;7(9):e45818.
17. Zeiger AS, Loe FC, Li R, Raghunath M, Van Vliet KJ. Macromolecular crowding directs extracellular matrix organization and mesenchymal stem cell behavior. PLoS One 2012;7(5):e37904.
18. Jerusalem A, Dao M. Continuum modeling of a neuronal cell under blast loading. Acta Biomater 2012;8(9):3360-3371.
19. Donnelly E. Methods for assessing bone quality: A review. Clin Orthop Relat Res 2011;469(8):2128-2138.
20. El-Safty S, Akhtar R, Silikas N, Watts DC. Nanomechanical properties of dental resin-composites. Dent Mater 2012;28(12):1292-1300.
21. Pathak S, Swadener JG, Kalidindi SR, Courtland HW, Jepsen KJ, Goldman HM. Measuring the dynamic mechanical response of hydrated mouse bone by nanoindentation. J Mech Behav Biomed Mater 2011;4(1):34-43.
22. Ho SP, Balooch M, Goodis HE, Marshall GW, Marshall SJ. Ultrastructure and nanomechanical properties of cementum dentin junction. J Biomed Mater Res A 2004;68A(2):343-351.
23. Katti KS, Mohanty B, Katti DR. Nanomechanical properties of nacre. J Mater Res 2006;21(5):1237-1242.
24. Mohanty B, Katti KS, Katti DR, Verma D. Dynamic nanomechanical response of nacre. J Mater Res 2006;21(8):2045-2051.
25. Suresh S. Biomechanics and biophysics of cancer cells. Acta Biomater 2007;3(4):413-438.
26. Chen J. Nanobiomechanics of living cells: A review. Interface Focus 2014;4(2):20130055.
27. Pharr GM, Oliver WC. Nanoindentation of silver-relations between hardness and dislocation-structure. J Mater Res 1989;4(1):94-101.
28. 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(12):1259-1266.
29. Oyen M, Taylor D. Special issue on nanoindentation of biological materials. J Mech Behav Biomed Mater 2009;2(4):311.
30. Shinto H, Aso Y, Fukasawa T, Higashitani K. Adhesion of melanoma cells to the surfaces of microspheres studied by atomic force microscopy. Colloids Surf B Biointerfaces 2012;91:114-121.
31. Heinrich C, Waas AM, Wineman AS. Determination of material properties using nanoindentation and multiple indenter tips. Inter J Solids Struct 2009;46(2):364-376.
32. Haydon P, Lartius R, Parpura V, Marchese-Ragona S. Membrane deformation of living glial cells using atomic force microscopy. J Microsc 1996;182:114-120.
33. Kirmizis D, Logothetidis S. Atomic force microscopy probing in the measurement of cell mechanics. Int J Nanomed 2010;5:137-145.
34. Tan JC, Furman JD, Cheetham AK. Relating mechanical properties and chemical bonding in an inorganic-organic framework material: A single-crystal nanoindentation study. J Am Chem Soc 2009;131(40):14252-14254.
35. Lewis G, Nyman JS. The use of nanoindentation for characterizing the properties of mineralized hard tissues: state-of-the art review. J Biomed Mater Res B 2008;87(1):286-301.
36. Putman CA, van der Werf KO, de Grooth BG, van Hulst NF, Greve J. Viscoelasticity of living cells allows high resolution imaging by tapping mode atomic force microscopy. Biophys J 1994;67(4):1749-1753.
37. Radmacher M, Fritz M, Kacher CM, Cleveland JP, Hansma PK. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys J 1996;70(1):556-567.
38. Radmacher M, Tillmann RW, Gaub HE. Imaging viscoelasticity by force modulation with the atomic force microscope. Biophys J 1993;64(3):735-742.
39. Chen J, Lu G. Finite element modelling of nanoindentation based methods for mechanical properties of cells. J Biomech 2012;45(16):2810-2816.
40. Sunbuloglu E, Bozdag E, Toprak T, Islak C. Experimental parameter estimation method for nonlinear viscoelastic composite material models: An application on arterial tissue. Comp Meth Biomech Biomed Eng 2013;16(12):1249-1261.
41. Chen D-L, Yang P-Y, Lai Y-S. A review of three-dimensional viscoelastic models with an application to viscoelasticity characterization using nanoindentation. Microelectr Reliab 2012;52(3):541-558.
42. Murphy MF, Lilley F, Lalor MJ, Crosby SR, Madden G, Johnston G, Burton DR. Evaluation of a nonlinear Hertzian-based model reveals prostate cancer cells respond differently to force than normal prostate cells. Microsc Res Tech 2013;76(1):36-41.
43. Jin Tong JS, Jiang Zhou. Nanoindentation of biomaterials handbook of nanophysics. Boca Raton, FL: CRC Press; 2010. p. 1-16.
44. Weisenhorn AL, Khorsandi M, Kasas S, Gotzos V, Butt H. Deformation and height anomaly of soft surfaces studied with an AFM. Nanotechnology 1993;4:106-113.
45. Fuhrmann A, Staunton JR, Nandakumar V, Banyai N, Davies PC, Ros R. AFM stiffness nanotomography of normal, metaplastic and dysplastic human esophageal cells. Phys Biol 2011;8(1):015007.
46. Lee MH, Wu PH, Staunton JR, Ros R, Longmore GD, Wirtz D. Mismatch in mechanical and adhesive properties induces pulsating cancer cell migration in epithelial monolayer. Biophys J 2012;102(12):2731-2741.
47. Lekka M, Laidler P, Labedz M, Kulik AJ, Lekki J, Zajac W, Stachura Z. Specific detection of glycans on a plasma membrane of living cells with atomic force microscopy. Chem Biol 2006;13(5):505-512.
48. Targosz-Korecka M, Biedron R, Szczygiel AM, Brzezinka G, Szczerbinski J, Zuk A. Stiffness changes of tumor HEp2 cells correlates with the inhibition and release of TRAIL-induced apoptosis pathways. J Mol Recognition 2012;25(5):299-308.
49. Khanna R, Katti KS, Katti DR. Experiments in nanomechanical properties of live osteoblast cells and cell-biomaterial interface. J Nanotechnol Eng Med 2012;2(4):041005 (Pages 041013).
50. Khanna R, Katti DR, Katti KS. AFM and nanoindentation studies of bone nodules on chitosan-polygalacturonic acid-hydroxyapatite nanocomposites. Comp Mod Eng Sci 2012;87(6):530-555.
51. Garcia-Tunon E, Couceiro R, Franco J, Saiz E, Guitian F. Synthesis and characterisation of large chlorapatite single-crystals with controlled morphology and surface roughness. J Mater Sci Mater Med 2012;23(10):2471-2482.
52. Docheva D, Padula D, Schieker M, Clausen-Schaumann H. Effect of collagen I and fibronectin on the adhesion, elasticity and cytoskeletal organization of prostate cancer cells. Biochem Biophys Res Commun 2010;402(2):361-366.
53. Kossivas F, Angeli S, Kafouris D, Patrickios CS, Tzagarakis V, Constantinides C. MRI-based morphological modeling, synthesis and characterization of cardiac tissue-mimicking materials. Biomed Mater 2012;7(3):035006.
54. Wang Y, Zhang L, Sun L, Webster TJ. Increased healthy osteoblast to osteosarcoma density ratios on specific PLGA nanopatterns. Int J Nanomed 2013;8:159-166.
55. Khanna R, Katti DR, Katti KS. Experiments in nanomechanical properties of live osteoblast cells and cell-biomaterial interface. J Nanotech Eng Med 2012;2:13.
56. Horimizu M, Kawase T, Tanaka T, Okuda K, Nagata M, Burns DM, Yoshie H. Biomechanical evaluation by AFM of cultured human cell-multilayered periosteal sheets. Micron 2013;48:1-10.
57. Codan B, Martinelli V, Mestroni L, Sbaizero O. Atomic force microscopy of 3T3 and SW-13 cell lines: An investigation of cell elasticity changes due to fixation. Mater Sci Eng C 2013;33(6):3303-3308.
58. McNamee CE, Pyo N, Higashitani K. Atomic force microscopy study of the specific adhesion between a colloid particle and a living melanoma cell: Effect of the charge and the hydrophobicity of the particle surface. Biophys J 2006;91(5):1960-1969.
59. Guo Q, Xia Y, Sandig M, Yang J. Characterization of cell elasticity correlated with cell morphology by atomic force microscope. J Biomech 2012;45(2):304-309.
60. Kim Y, Stolarska MA, Othmer HG. The role of the microenvironment in tumor growth and invasion. Prog Biophys Mol Biol 2011;106(2):353-379.
61. Ingber DE. Can cancer be reversed by engineering the tumor microenvironment? Semin Cancer Biol 2008;18(5):356-364.
62. Wu Y, McEwen GD, Harihar S, Baker SM, DeWald DB, Zhou A. BRMS1 expression alters the ultrastructural, biomechanical and biochemical properties of MDA-MB-435 human breast carcinoma cells: An AFM and Raman microspectroscopy study. Cancer Lett 2010;293(1):82-91.
63. Leight JL, Wozniak MA, Chen S, Lynch ML, Chen CS. Matrix rigidity regulates a switch between TGF-beta1-induced apoptosis and epithelial-mesenchymal transition. Mol Biol Cell 2012;23(5):781-791.
64. Li M, Liu L, Xi N, Wang Y, Dong Z, Tabata O, Xiao X, Zhang W. Imaging and measuring the rituximab-induced changes of mechanical properties in B-lymphoma cells using atomic force microscopy. Biochem Biophys Res Commun 2011;404(2):689-694.
65. Li M, Xiao X, Liu L, Xi N, Wang Y, Dong Z, Zhang W. Atomic force microscopy study of the antigen-antibody binding force on patient cancer cells based on ROR1 fluorescence recognition. J Mol Recognit 2013;26(9):432-438.
66. Valbuena A, Vera AM, Oroz J, Menendez M, Carrion-Vazquez M. Mechanical properties of beta-catenin revealed by single-molecule experiments. Biophys J 2012;103(8):1744-1752.
67. Kumar S, Weaver VM. Mechanics, malignancy, and metastasis: The force journey of a tumor cell. Cancer Metastasis Rev 2009;28(1-2):113-127.
68. Cross SE, Jin YS, Rao J, Gimzewski JK. Nanomechanical analysis of cells from cancer patients. Nature Nanotech 2007;2(12):780-783.
69. Cross SE, Jin YS, Tondre J, Wong R, Rao J, Gimzewski JK. AFM-based analysis of human metastatic cancer cells. Nanotechnology 2008;19(38):384003.
70. Iwao K, Matoba R, Ueno N, Ando A, Miyoshi Y, Matsubara K, Noguchi S, Kato K. Molecular classification of primary breast tumors possessing distinct prognostic properties. Hum Mol Genet 2002;11(2):199-206.
71. Hu K, Zhao F, Wang Q. Mechanical characterization of living and dead undifferentiated human adipose-derived stem cells by using atomic force microscopy. Proc Inst Mech Eng H 2013; 227:1319-1323.
72. Ahn BM, Kim J, Ian L, Rha KH, Kim HJ. Mechanical property characterization of prostate cancer using a minimally motorized indenter in an ex vivo indentation experiment. Urology 2010;76(4):1007-1011.
73. Wilson SL, Guilbert M, Sule-Suso J, Torbet J, Jeannesson P, Sockalingum GD, Yang Y. A microscopic and macroscopic study of aging collagen on its molecular structure, mechanical properties, and cellular response. FASEB J 2014;28(1):14-25.
74. Wilson SL, Yang Y, El Haj AJ. Corneal stromal cell plasticity: In vitro regulation of cell phenotype through cell-cell interactions in a three-dimensional model. Tissue Eng Part A 2014;20(1-2):225-238.
75. Wang Y, Insana MF. Viscoelastic properties of rodent mammary tumors using ultrasonic shear-wave imaging. Ultrason Imaging 2013;35(2):126-145.
76. Zhou Z, Zheng C, Li S, Zhou X, Liu Z, He Q, Zhang N, Ngan A, Tang B, Wang A. AFM nanoindentation detection of the elastic modulus of tongue squamous carcinoma cells with different metastatic potentials. Nanomedicine 2013; 9:864-874.
77. Sariisik E, Docheva D, Padula D, Popov C, Opfer J, Schieker M, Clausen-Schaumann H, Benoit M. Probing the interaction forces of prostate cancer cells with collagen I and bone marrow derived stem cells on the single cell level. PLoS One 2013;8(3):e57706.
78. Wing-Han Yuen Q, Zheng YP, Huang YP, He JF, Chung-Wai Cheung J, Ying M. In-vitro strain and modulus measurements in porcine cervical lymph nodes. Open Biomed Eng J 2011;5:39-46.
79. Lekka M, Gil D, Pogoda K, Dulinska-Litewka J, Jach R, Gostek J, Klymenko O, Prauzner-Bechcicki S, Stachura Z, Wiltowska-Zuber J, Okon K, Laidler P. Cancer cell detection in tissue sections using AFM. Arch Bioch Biophys 2012;518(2):151-156.
80. Prabhune M, Belge G, Dotzauer A, Bullerdiek J, Radmacher M. Comparison of mechanical properties of normal and malignant thyroid cells. Micron 2012;43(12):1267-1272.
81. Rosenbluth MJ, Lam WA, Fletcher DA. Force microscopy of nonadherent cells: A comparison of leukemia cell deformability. Biophys J 2006;90(8):2994-3003.
82. Roberts PC, Mottillo EP, Baxa AC, Heng HH, Doyon-Reale N, Gregoire L, Lancaster WD, Rabah R, Schmelz EM. Sequential molecular and cellular events during neoplastic progression: A mouse syngeneic ovarian cancer model. Neoplasia 2005;7(10):944-956.
83. Ketene AN, Roberts PC, Shea AA, Schmelz EM, Agah M. Actin filaments play a primary role for structural integrity and viscoelastic response in cells. Integr Biol 2012;4(5):540-549.
84. Strobl JS, Nikkhah M, Agah M. Actions of the anti-cancer drug suberoylanilide hydroxamic acid (SAHA) on human breast cancer cytoarchitecture in silicon microstructures. Biomaterials 2010;31(27):7043-7050.
85. Beenakker JW, Ashcroft BA, Lindeman JH, Oosterkamp TH. Mechanical properties of the extracellular matrix of the aorta studied by enzymatic treatments. Biophys J 2012;102(8):1731-1737.
86. Pradhan SM, Katti KS, Katti DR. Structural hierarchy controls deformation behavior of collagen. Biomacromolecules 2012;13(8):2562-2569.
87. Sadeghi Naini A, Patel RV, Samani A. Measurement of lung hyperelastic properties using inverse finite element approach. IEEE Trans Biomed Eng 2011;58(10):2852-2859.
88. Baker EL, Lu J, Yu D, Bonnecaze RT, Zaman MH. Cancer cell stiffness: Integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys J 2010;99(7):2048-2057.
89. Karagiannis GS, Poutahidis T, Erdman SE, Kirsch R, Riddell RH, Diamandis EP. Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol Cancer Res 2012;10(11):1403-1418.
90. Rauch C. On the relationship between drug's size, cell membrane mechanical properties and high levels of multi drug resistance: A comparison to published data. Eur Biophys J 2009;38(4):537-546.
91. Lam WA, Rosenbluth MJ, Fletcher DA. Chemotherapy exposure increases leukemia cell stiffness. Blood 2007;109(8):3505-3508.
92. El Kaffas A, Bekah D, Rui M, Kumaradas JC, Kolios MC. Investigating longitudinal changes in the mechanical properties of MCF-7 cells exposed to paclitaxol using particle tracking microrheology. Phys Med Biol 2013;58(4):923-936.
93. Zhang D, Kilian KA. The effect of mesenchymal stem cell shape on the maintenance of multipotency. Biomaterials 2013;34(16):3962-3969.
94. Lee J, Abdeen AA, Zhang D, Kilian KA. Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition. Biomaterials 2013;34(33):8140-8148.
95. Cai X, Xing X, Cai J, Chen Q, Wu S, Huang F. Connection between biomechanics and cytoskeleton structure of lymphocyte and Jurkat cells: An AFM study. Micron 2010;41(3):257-262.
96. Sharma S, Santiskulvong C, Bentolila LA, Rao J, Dorigo O, Gimzewski JK. Correlative nanomechanical profiling with super-resolution F-actin imaging reveals novel insights into mechanisms of cisplatin resistance in ovarian cancer cells. Nanomedicine 2012;8(5):757-766.
97. Kao FS, Pan YR, Hsu RQ, Chen HM. Efficacy verification and microscopic observations of an anticancer peptide, CB1a, on single lung cancer cell. Biochim Biophys Acta 2012;1818(12):2927-2935.
98. Hendricks P, Diaz FJ, Schmitt S, Sitta Sittampalam G, Nirmalanandhan VS. Effects of respiratory mechanical forces on the pharmacological response of lung cancer cells to chemotherapeutic agents. Fundam Clin Pharm 2012;26(5):632-643.
99. Saab MB, Bec N, Martin M, Estephan E, Cuisinier F, Larroque C, Gergely C. Differential effect of curcumin on the nanomechanics of normal and cancerous Mammalian epithelial cells. Cell Biochem Biophys 2013;65(3):399-411.
100. Saab MB, Estephan E, Bec N, Larroque M, Aulombard R, Cloitre T, Gergely C. Multimicroscopic study of curcumin effect on fixed nonmalignant and cancerous mammalian epithelial cells. J Biophotonics 2011;4(7-8):533-543.
101. Cross SE, Jin YS, Lu QY, Rao J, Gimzewski JK. Green tea extract selectively targets nanomechanics of live metastatic cancer cells. Nanotechnology 2011;22(21):215101.
102. Watanabe T, Kuramochi H, Takahashi A, Imai K, Katsuta N, Nakayama T, Fujiki H, Suganuma M. Higher cell stiffness indicating lower metastatic potential in B16 melanoma cell variants and in (-)-epigallocatechin gallate-treated cells. J Cancer Res Clin Oncol 2012;138:859-866.
103. Yallapu MM, Dobberpuhl MR, Maher DM, Jaggi M, Chauhan SC. Design of curcumin loaded cellulose nanoparticles for prostate cancer. Curr Drug Metab 2012;13(1):120-128.
104. Yallapu MM, Ebeling MC, Chauhan N, Jaggi M, Chauhan SC. Interaction of curcumin nanoformulations with human plasma proteins and erythrocytes. Int J Nanomed 2011;6:2779-2790.
105. Yallapu MM, Ebeling MC, Khan S, Sundram V, Chauhan N, Gupta BK, Puumala SE, Jaggi M, Chauhan SC. Novel curcumin-loaded magnetic nanoparticles for pancreatic cancer treatment. Mol Cancer Ther 2013;12(8):1471-1480.
106. Yallapu MM, Gupta BK, Jaggi M, Chauhan SC. Fabrication of curcumin encapsulated PLGA nanoparticles for improved therapeutic effects in metastatic cancer cells. J Colloid Interface Sci 2010;351(1):19-29.
107. Yallapu MM, Jaggi M, Chauhan SC. Curcumin nanomedicine: A road to cancer therapeutics. Curr Pharm Des 2013;19(11):1994-2010.
108. Yallapu MM, Maher DM, Sundram V, Bell MC, Jaggi M, Chauhan SC. Curcumin induces chemo/radio-sensitization in ovarian cancer cells and curcumin nanoparticles inhibit ovarian cancer cell growth. J Ovarian Res 2010;3:11.
109. Yang F, Jin H, Pi J, Jiang JH, Liu L, Bai HH, Yang PH, Cai JY. Anti-tumor activity evaluation of novel chrysin-organogermanium(IV) complex in MCF-7 cells. Bioorg Med Chem Lett 2013;23(20):5544-5551.
110. Koczurkiewicz P, Podolak I, Skrzeczynska-Moncznik J, Sarna M, Wojcik KA, Ryszawy D, Galanty A, Lasota S, Madeja Z, Czyz J, Michalik M. Triterpene saponosides from Lysimachia ciliata differentially attenuate invasive potential of prostate cancer cells. Chem Biol Interact 2013;206(1):6-17.
111. Kuo WT, Dong GC, Yao CH, Huang JY, Lin FH. Evaluation of adhesion force and binding affinity of phytohemagglutinin erythroagglutinating to EGF receptor on human lung cancer cells. Curr Med Chem 2013;20(19):2476-2485.
112. Pelling AE, Dawson DW, Carreon DM, Christiansen JJ, Shen RR, Teitell MA, Gimzewski JK. Distinct contributions of microtubule subtypes to cell membrane shape and stability. Nanomedicine 2007;3(1):43-52.
113. Pi J, Yang F, Jin H, Huang X, Liu R, Yang P, Cai J. Selenium nanoparticles induced membrane bio-mechanical property changes in MCF-7 cells by disturbing membrane molecules and F-actin. Bioorg Med Chem Lett 2013;23(23):6296-6303.
114. Vasir JK, Labhasetwar V. Quantification of the force of nanoparticle-cell membrane interactions and its influence on intracellular trafficking of nanoparticles. Biomaterials 2008;29(31):4244-4252.
115. Turkcan S, Richly MU, Bouzigues CI, Allain JM, Alexandrou A. Receptor displacement in the cell membrane by hydrodynamic force amplification through nanoparticles. Biophys J 2013;105(1):116-126.
116. Chaudhuri A, Battaglia G, Golestanian R. The effect of interactions on the cellular uptake of nanoparticles. Phys Biol 2011;8(4):046002.
117. Peetla C, Labhasetwar V. Effect of molecular structure of cationic surfactants on biophysical interactions of surfactant-modified nanoparticles with a model membrane and cellular uptake. Langmuir 2009;25(4):2369-2377.
118. Samani A, Plewes D. A method to measure the hyperelastic parameters of ex vivo breast tissue samples. Phys Med Biol 2004;49(18):4395-4405.
119. Yang TH, Leung SK, Phipps S, Reuben RL, McNeill SA, Habib FK, Schnieder A, Stevens R. In-vitro dynamic micro-probing and the mechanical properties of human prostate tissues. Technol Health Care 2006;14(4-5):281-296.
120. Jalkanen V, Andersson BM, Bergh A, Ljungberg B, Lindahl OA. Indentation loading response of a resonance sensor-discriminating prostate cancer and normal tissue. J Med Eng Technol 2013;37(7):416-423.
121. Shin TY, Kim YJ, Lim SK, Kim J, Rha KH. Robotic mechanical localization of prostate cancer correlates with magnetic resonance imaging scans. Yonsei Med J 2013;54(4):907-911.
122. Ichinose J, Kohno T, Fujimori S, Harano T, Suzuki S, Fujii T. Invasiveness and malignant potential of pulmonary lesions presenting as pure ground-glass opacities. Ann Thorac Cardiovasc Surg 2013; http://dx.doi.org/10.5761/atcs.oa.13-00005.
123. Nazarian A, von Stechow D, Zurakowski D, Muller R, Snyder BD. Bone volume fraction explains the variation in strength and stiffness of cancellous bone affected by metastatic cancer and osteoporosis. Calcif Tissue Int 2008;83(6):368-379.
124. Plodinec M, Loparic M, Monnier CA, Obermann EC, Zanetti-Dallenbach R, Oertle P, Hyotyla JT, Aebi U, Bentires-Alj M, Lim RY, Schoenenberger CA. The nanomechanical signature of breast cancer. Nat Nanotech 2012;7(11):757-765.
125. Kim MS, Kim J, Lee W, Cho SJ, Oh JM, Lee JY, Baek S, Kim YJ, Sim TS, Lee HJ, Jung GE, Kim SI, Park JM, Oh JH, Gurel O, Lee SS, Lee JG. A trachea-inspired bifurcated microfilter capturing viable circulating tumor cells via altered biophysical properties as measured by atomic force microscopy. Small 2013;9(18):3103-3110.
126. Sarna M, Zadlo A, Pilat A, Olchawa M, Gkogkolou P, Burda K, Bohm M, Sarna T. Nanomechanical analysis of pigmented human melanoma cells. Pigment Cell Melanoma Res 2013;26(5):727-730.