The Roles of Cellular Nanomechanics in Cancer

The biomechanical properties of cells and tissues may be instrumental in increasing our understanding of cellular behavior and cellular manifestations of diseases such as cancer. Nanomechanical properties can offer clinical translation of therapies beyond what are currently employed. Nanomechanical properties, often measured by nanoindentation methods using atomic force microscopy, may identify morphological variations, cellular binding forces, and surface adhesion behaviors that efficiently differentiate normal cells and cancer cells. The aim of this review is to examine current research involving the general use of atomic force microscopy/nanoindentation in measuring cellular nanomechanics; various factors and instrumental conditions that influence the nanomechanical properties of cells; and implementation of nanoindentation methods to distinguish cancer cells from normal cells or tissues. Applying these fundamental nanomechanical properties to current discoveries in clinical treatment may result in greater efficiency in diagnosis, treatment, and prevention of cancer, which ultimately can change the lives of patients.

[1]  Qingkang Wang,et al.  Mechanical characterization of living and dead undifferentiated human adipose-derived stem cells by using atomic force microscopy , 2013, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[2]  Abbas Samani,et al.  A method to measure the hyperelastic parameters of ex vivo breast tissue samples. , 2004, Physics in medicine and biology.

[3]  Ratnesh Lal,et al.  Multidimensional atomic force microscopy for drug discovery: a versatile tool for defining targets, designing therapeutics and monitoring their efficacy. , 2010, Life sciences.

[4]  N. Dubrawsky Cancer statistics , 1989, CA: a cancer journal for clinicians.

[5]  D. Docheva,et al.  Probing the Interaction Forces of Prostate Cancer Cells with Collagen I and Bone Marrow Derived Stem Cells on the Single Cell Level , 2013, PloS one.

[6]  M. Lalor,et al.  Evaluation of a nonlinear Hertzian‐based model reveals prostate cancer cells respond differently to force than normal prostate cells , 2013, Microscopy research and technique.

[7]  G. Lu,et al.  Finite element modelling of nanoindentation based methods for mechanical properties of cells. , 2012, Journal of biomechanics.

[8]  E. Bozdag,et al.  Experimental Parameter Estimation Method for Nonlinear Viscoelastic Composite Material Models: An Application on Arterial Tissue , 2013, Computer methods in biomechanics and biomedical engineering.

[9]  James K Gimzewski,et al.  Green tea extract selectively targets nanomechanics of live metastatic cancer cells , 2011, Nanotechnology.

[10]  J. Beenakker,et al.  Mechanical properties of the extracellular matrix of the aorta studied by enzymatic treatments. , 2012, Biophysical journal.

[11]  Michael F Insana,et al.  Viscoelastic Properties of Rodent Mammary Tumors Using Ultrasonic Shear-Wave Imaging , 2013, Ultrasonic imaging.

[12]  Daniel A Fletcher,et al.  Chemotherapy exposure increases leukemia cell stiffness. , 2007, Blood.

[13]  Qin Tu,et al.  Atomic force microscope study of tumor cell membranes following treatment with anti-cancer drugs. , 2009, Biosensors & bioelectronics.

[14]  N. Bec,et al.  Differential Effect of Curcumin on the Nanomechanics of Normal and Cancerous Mammalian Epithelial Cells , 2012, Cell Biochemistry and Biophysics.

[15]  N. Chauhan,et al.  Novel Curcumin-Loaded Magnetic Nanoparticles for Pancreatic Cancer Treatment , 2013, Molecular Cancer Therapeutics.

[16]  K. Higashitani,et al.  Adhesion of melanoma cells to the surfaces of microspheres studied by atomic force microscopy. , 2012, Colloids and surfaces. B, Biointerfaces.

[17]  Flavien Pillet,et al.  Atomic Force Microscopy and pharmacology: from microbiology to cancerology. , 2014, Biochimica et biophysica acta.

[18]  V. Labhasetwar,et al.  Effect of molecular structure of cationic surfactants on biophysical interactions of surfactant-modified nanoparticles with a model membrane and cellular uptake. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[19]  E. Schmelz,et al.  Biomechanical profile of cancer stem-like/tumor-initiating cells derived from a progressive ovarian cancer model. , 2014, Nanomedicine : nanotechnology, biology, and medicine.

[20]  M. Lekka,et al.  Specific detection of glycans on a plasma membrane of living cells with atomic force microscopy. , 2006, Chemistry & biology.

[21]  Lianqing Liu,et al.  Imaging and measuring the rituximab-induced changes of mechanical properties in B-lymphoma cells using atomic force microscopy. , 2011, Biochemical and biophysical research communications.

[22]  C. Schuh Nanoindentation studies of materials , 2006 .

[23]  G. Marshall,et al.  Ultrastructure and nanomechanical properties of cementum dentin junction. , 2004, Journal of biomedical materials research. Part A.

[24]  James K Gimzewski,et al.  Correlative nanomechanical profiling with super-resolution F-actin imaging reveals novel insights into mechanisms of cisplatin resistance in ovarian cancer cells. , 2012, Nanomedicine : nanotechnology, biology, and medicine.

[25]  M. Carrión-Vázquez,et al.  Mechanical properties of β-catenin revealed by single-molecule experiments. , 2012, Biophysical journal.

[26]  Murali M. Yallapu,et al.  Interaction of curcumin nanoformulations with human plasma proteins and erythrocytes , 2011, International journal of nanomedicine.

[27]  S. Chizhik,et al.  Atomic force microscopy probing of cell elasticity. , 2007, Micron.

[28]  Stefan Schinkinger,et al.  Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. , 2005, Biophysical journal.

[29]  Samantha L Wilson,et al.  Corneal stromal cell plasticity: in vitro regulation of cell phenotype through cell-cell interactions in a three-dimensional model. , 2014, Tissue engineering. Part A.

[30]  R. Akhtar,et al.  Nanomechanical properties of dental resin-composites. , 2012, Dental materials : official publication of the Academy of Dental Materials.

[31]  A. Jemal,et al.  Cancer statistics, 2013 , 2013, CA: a cancer journal for clinicians.

[32]  Yeongjin Kim,et al.  Robotic Mechanical Localization of Prostate Cancer Correlates with Magnetic Resonance Imaging Scans , 2013, Yonsei medical journal.

[33]  K. Higashitani,et al.  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. , 2006, Biophysical journal.

[34]  K. Katti,et al.  Nanomechanical properties of nacre , 2006 .

[35]  M. Oyen,et al.  Special issue on nanoindentation of biological materials. , 2009, Journal of the mechanical behavior of biomedical materials.

[36]  O Sbaizero,et al.  Atomic force microscopy of 3T3 and SW-13 cell lines: an investigation of cell elasticity changes due to fixation. , 2013, Materials science & engineering. C, Materials for biological applications.

[37]  M. Lekka,et al.  Cancer cell recognition--mechanical phenotype. , 2012, Micron.

[38]  Z. Madeja,et al.  Triterpene saponosides from Lysimachia ciliata differentially attenuate invasive potential of prostate cancer cells. , 2013, Chemico-biological interactions.

[39]  Ueli Aebi,et al.  The nanomechanical signature of breast cancer. , 2012, Nature nanotechnology.

[40]  Jiye Cai,et al.  Selenium nanoparticles induced membrane bio-mechanical property changes in MCF-7 cells by disturbing membrane molecules and F-actin. , 2013, Bioorganic & medicinal chemistry letters.

[41]  Gladius Lewis,et al.  The use of nanoindentation for characterizing the properties of mineralized hard tissues: state-of-the art review. , 2008, Journal of biomedical materials research. Part B, Applied biomaterials.

[42]  Ning Xi,et al.  The Emergence of AFM Applications to Cell Biology: How new technologies are facilitating investigation of human cells in health and disease at the nanoscale. , 2011, Journal of nanoscience letters.

[43]  M. Nikkhah,et al.  Actions of the anti-cancer drug suberoylanilide hydroxamic acid (SAHA) on human breast cancer cytoarchitecture in silicon microstructures. , 2010, Biomaterials.

[44]  Daniel J Müller,et al.  Atomic force microscopy: a nanoscopic window on the cell surface. , 2011, Trends in cell biology.

[45]  Silvan Türkcan,et al.  Receptor displacement in the cell membrane by hydrodynamic force amplification through nanoparticles. , 2013, Biophysical journal.

[46]  Shinzaburo Noguchi,et al.  Molecular classification of primary breast tumors possessing distinct prognostic properties. , 2002, Human molecular genetics.

[47]  Zbigniew Stachura,et al.  Cancer cell detection in tissue sections using AFM. , 2012, Archives of biochemistry and biophysics.

[48]  K. Katti,et al.  Dynamic nanomechanical response of nacre , 2006 .

[49]  H. Heng,et al.  Sequential molecular and cellular events during neoplastic progression: a mouse syngeneic ovarian cancer model. , 2005, Neoplasia.

[50]  나군호,et al.  Mechanical property characterization of prostate cancer using a minimally motorized indenter in an ex vivo indentation experiment , 2010 .

[51]  Yu-Zhong Zhang,et al.  Antimicrobial Peptide Trichokonin VI-Induced Alterations in the Morphological and Nanomechanical Properties of Bacillus subtilis , 2012, PloS one.

[52]  김승일 A Trachea-Inspired Bifurcated Microfilter Capturing Viable Circulating Tumor Cells via Altered Biophysical Properties as Measured by Atomic Force Microscopy , 2013 .

[53]  M. Radmacher,et al.  Imaging viscoelasticity by force modulation with the atomic force microscope. , 1993, Biophysical journal.

[54]  Murali M. Yallapu,et al.  Fabrication of curcumin encapsulated PLGA nanoparticles for improved therapeutic effects in metastatic cancer cells. , 2010, Journal of colloid and interface science.

[55]  Qiuquan Guo,et al.  Characterization of cell elasticity correlated with cell morphology by atomic force microscope. , 2012, Journal of biomechanics.

[56]  Daniel A Fletcher,et al.  Force microscopy of nonadherent cells: a comparison of leukemia cell deformability. , 2006, Biophysical journal.

[57]  T. Kohno,et al.  Invasiveness and malignant potential of pulmonary lesions presenting as pure ground-glass opacities. , 2014, Annals of thoracic and cardiovascular surgery : official journal of the Association of Thoracic and Cardiovascular Surgeons of Asia.

[58]  B. Ahn,et al.  Mechanical property characterization of prostate cancer using a minimally motorized indenter in an ex vivo indentation experiment. , 2010, Urology.

[59]  V. Labhasetwar,et al.  Quantification of the force of nanoparticle-cell membrane interactions and its influence on intracellular trafficking of nanoparticles. , 2008, Biomaterials.

[60]  Jinju Chen,et al.  Nanobiomechanics of living cells: a review , 2014, Interface Focus.

[61]  K. Katti,et al.  Structural hierarchy controls deformation behavior of collagen. , 2012, Biomacromolecules.

[62]  K. Katti,et al.  Experiments in Nanomechanical Properties of Live Osteoblast Cells and Cell–Biomaterial Interface , 2011 .

[63]  M. Jaggi,et al.  Design of curcumin loaded cellulose nanoparticles for prostate cancer. , 2012, Current drug metabolism.

[64]  D. Docheva,et al.  Effect of collagen I and fibronectin on the adhesion, elasticity and cytoskeletal organization of prostate cancer cells. , 2010, Biochemical and biophysical research communications.

[65]  Robert M Henderson,et al.  Atomic force microscopy and drug discovery. , 2004, Drug discovery today.

[66]  Subra Suresh,et al.  Biomechanics and biophysics of cancer cells. , 2007, Acta biomaterialia.

[67]  Dihua Yu,et al.  Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential. , 2010, Biophysical journal.

[68]  Minseok S Kim,et al.  A trachea-inspired bifurcated microfilter capturing viable circulating tumor cells via altered biophysical properties as measured by atomic force microscopy. , 2013, Small.

[69]  Hans G Othmer,et al.  The role of the microenvironment in tumor growth and invasion. , 2011, Progress in biophysics and molecular biology.

[70]  Jiye Cai,et al.  Connection between biomechanics and cytoskeleton structure of lymphocyte and Jurkat cells: An AFM study. , 2010, Micron.

[71]  Murali M. Yallapu,et al.  Curcumin nanomedicine: a road to cancer therapeutics. , 2013, Current pharmaceutical design.

[72]  V. Parpura,et al.  Membrane deformation of living glial cells using atomic force microscopy , 1996, Journal of microscopy.

[73]  B G de Grooth,et al.  Viscoelasticity of living cells allows high resolution imaging by tapping mode atomic force microscopy. , 1994, Biophysical journal.

[74]  J. Gimzewski,et al.  Distinct contributions of microtubule subtypes to cell membrane shape and stability. , 2007, Nanomedicine : nanotechnology, biology, and medicine.

[75]  James K Gimzewski,et al.  AFM-based analysis of human metastatic cancer cells , 2008, Nanotechnology.

[76]  R. Hsu,et al.  Efficacy verification and microscopic observations of an anticancer peptide, CB1a, on single lung cancer cell. , 2012, Biochimica et biophysica acta.

[77]  Y. Zheng,et al.  In-vitro Strain and Modulus Measurements in Porcine Cervical Lymph Nodes , 2011, The open biomedical engineering journal.

[78]  Agnieszka Szczygieł,et al.  Stiffness changes of tumor HEp2 cells correlates with the inhibition and release of TRAIL‐induced apoptosis pathways , 2012, Journal of molecular recognition : JMR.

[79]  Donald E Ingber,et al.  Can cancer be reversed by engineering the tumor microenvironment? , 2008, Seminars in cancer biology.

[80]  Rajnikant V. Patel,et al.  Measurement of Lung Hyperelastic Properties Using Inverse Finite Element Approach , 2011, IEEE Transactions on Biomedical Engineering.

[81]  Sarah Schmitt,et al.  Effects of respiratory mechanical forces on the pharmacological response of lung cancer cells to chemotherapeutic agents , 2012, Fundamental & clinical pharmacology.

[82]  B. Snyder,et al.  Bone Volume Fraction Explains the Variation in Strength and Stiffness of Cancellous Bone Affected by Metastatic Cancer and Osteoporosis , 2008, Calcified Tissue International.

[83]  Douglas Zhang,et al.  The effect of mesenchymal stem cell shape on the maintenance of multipotency. , 2013, Biomaterials.

[84]  Z. Stachura,et al.  Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy , 1999, European Biophysics Journal.

[85]  Stergios Logothetidis,et al.  Atomic force microscopy probing in the measurement of cell mechanics , 2010, International journal of nanomedicine.

[86]  T. Webster,et al.  Increased healthy osteoblast to osteosarcoma density ratios on specific PLGA nanopatterns , 2013, International journal of nanomedicine.

[87]  Michael C. Kolios,et al.  Investigating longitudinal changes in the mechanical properties of MCF-7 cells exposed to paclitaxol using particle tracking microrheology , 2013, Physics in medicine and biology.

[88]  Sanjay Kumar,et al.  Mechanics, malignancy, and metastasis: The force journey of a tumor cell , 2009, Cancer and Metastasis Reviews.

[89]  K. Katti,et al.  AFM and Nanoindentation Studies of Bone Nodules on Chitosan-Polygalacturonic Acid-Hydroxyapatite Nanocomposites , 2012 .

[90]  Sandor Kasas,et al.  Deformation and height anomaly of soft surfaces studied with an AFM , 1993 .

[91]  D. M. Burns,et al.  Biomechanical evaluation by AFM of cultured human cell-multilayered periosteal sheets. , 2013, Micron.

[92]  Yi-Shao Lai,et al.  A review of three-dimensional viscoelastic models with an application to viscoelasticity characterization using nanoindentation , 2012, Microelectron. Reliab..

[93]  N. Katsuta,et al.  Higher cell stiffness indicating lower metastatic potential in B16 melanoma cell variants and in (−)-epigallocatechin gallate-treated cells , 2012, Journal of Cancer Research and Clinical Oncology.

[94]  C. Rauch On the relationship between drug’s size, cell membrane mechanical properties and high levels of multi drug resistance: a comparison to published data , 2009, European Biophysics Journal.

[95]  N. Bec,et al.  Multimicroscopic study of curcumin effect on fixed nonmalignant and cancerous mammalian epithelial cells , 2011, Journal of biophotonics.

[96]  W. Charemza,et al.  Conclusions and future prospects , 1989 .

[97]  Adam S. Zeiger,et al.  Macromolecular Crowding Directs Extracellular Matrix Organization and Mesenchymal Stem Cell Behavior , 2012, PloS one.

[98]  Lianqing Liu,et al.  Atomic force microscopy study of the antigen‐antibody binding force on patient cancer cells based on ROR1 fluorescence recognition , 2013, Journal of molecular recognition : JMR.

[99]  K. Jepsen,et al.  Measuring the dynamic mechanical response of hydrated mouse bone by nanoindentation. , 2011, Journal of the mechanical behavior of biomedical materials.

[100]  A. Ngan,et al.  AFM nanoindentation detection of the elastic modulus of tongue squamous carcinoma cells with different metastatic potentials. , 2013, Nanomedicine : nanotechnology, biology, and medicine.

[101]  Christopher S. Chen,et al.  Matrix rigidity regulates a switch between TGF-β1–induced apoptosis and epithelial–mesenchymal transition , 2012, Molecular biology of the cell.

[102]  A. Cheetham,et al.  Relating mechanical properties and chemical bonding in an inorganic-organic framework material: a single-crystal nanoindentation study. , 2009, Journal of the American Chemical Society.

[103]  Markus Böhm,et al.  Nanomechanical analysis of pigmented human melanoma cells , 2013, Pigment cell & melanoma research.

[104]  Eleftherios P. Diamandis,et al.  Cancer-Associated Fibroblasts Drive the Progression of Metastasis through both Paracrine and Mechanical Pressure on Cancer Tissue , 2012, Molecular Cancer Research.

[105]  P K Hansma,et al.  Measuring the viscoelastic properties of human platelets with the atomic force microscope. , 1996, Biophysical journal.

[106]  Pei Yang,et al.  Anti-tumor activity evaluation of novel chrysin-organogermanium(IV) complex in MCF-7 cells. , 2013, Bioorganic & medicinal chemistry letters.

[107]  R L Reuben,et al.  In-vitro dynamic micro-probing and the mechanical properties of human prostate tissues. , 2006, Technology and health care : official journal of the European Society for Engineering and Medicine.

[108]  Eve Donnelly,et al.  Methods for Assessing Bone Quality: A Review , 2011, Clinical orthopaedics and related research.

[109]  C. Constantinides,et al.  MRI-based morphological modeling, synthesis and characterization of cardiac tissue-mimicking materials , 2012, Biomedical materials.

[110]  Manfred Radmacher,et al.  Comparison of mechanical properties of normal and malignant thyroid cells. , 2012, Micron.

[111]  J. Rao,et al.  Nanomechanical analysis of cells from cancer patients. , 2007, Nature nanotechnology.

[112]  E. Schmelz,et al.  Actin filaments play a primary role for structural integrity and viscoelastic response in cells. , 2012, Integrative biology : quantitative biosciences from nano to macro.

[113]  Ying Yang,et al.  A microscopic and macroscopic study of aging collagen on its molecular structure, mechanical properties, and cellular response , 2014, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[114]  Marc A. Meyers,et al.  Biological materials: Functional adaptations and bioinspired designs , 2012 .

[115]  A. Fuhrmann,et al.  AFM stiffness nanotomography of normal, metaplastic and dysplastic human esophageal cells , 2011, Physical biology.

[116]  Yangzhe Wu,et al.  BRMS1 expression alters the ultrastructural, biomechanical and biochemical properties of MDA-MB-435 human breast carcinoma cells: an AFM and Raman microspectroscopy study. , 2010, Cancer letters.

[117]  M A Meyers,et al.  Structure and mechanical properties of selected biological materials. , 2008, Journal of the mechanical behavior of biomedical materials.

[118]  A. Wineman,et al.  Determination of material properties using nanoindentation and multiple indenter tips , 2009 .

[119]  Ville Jalkanen,et al.  Indentation loading response of a resonance sensor—discriminating prostate cancer and normal tissue , 2013, Journal of medical engineering & technology.

[120]  R. Golestanian,et al.  The effect of interactions on the cellular uptake of nanoparticles , 2011, Physical biology.

[121]  G. Pharr,et al.  Nanoindentation of silver-relations between hardness and dislocation structure , 1989 .

[122]  Antoine Jérusalem,et al.  Continuum modeling of a neuronal cell under blast loading. , 2012, Acta biomaterialia.

[123]  Vasudha Sundram,et al.  Curcumin induces chemo/radio-sensitization in ovarian cancer cells and curcumin nanoparticles inhibit ovarian cancer cell growth , 2010, Journal of ovarian research.

[124]  Junmin Lee,et al.  Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition. , 2013, Biomaterials.

[125]  Denis Wirtz,et al.  Mismatch in mechanical and adhesive properties induces pulsating cancer cell migration in epithelial monolayer. , 2012, Biophysical journal.

[126]  E. Saiz,et al.  Synthesis and characterisation of large chlorapatite single-crystals with controlled morphology and surface roughness , 2012, Journal of Materials Science: Materials in Medicine.