Bidirectional mechanobiology between cells and their local extracellular matrix probed by atomic force microscopy

DuFort, 2011, Balancing forces: architectural control of mechanotransduction, Nat. Rev. Mol. Cell Biol., 12, 308, 10.1038/nrm3112 Ingber, 2003, Mechanobiology and diseases of mechanotransduction, Ann. Med., 35, 564, 10.1080/07853890310016333 Melo, 2014, Inhomogeneity of local stiffness in the extracellular matrix scaffold of fibrotic mouse lungs, J. Mech. Behav. Biomed. Mater., 37, 186, 10.1016/j.jmbbm.2014.05.019 Jorba, 2017, Ageing and chronic intermittent hypoxia mimicking sleep apnea do not modify local brain tissue stiffness in healthy mice, J. Mech. Behav. Biomed. Mater., 71, 106, 10.1016/j.jmbbm.2017.03.001 Butcher, 2009, A tense situation: forcing tumour progression, Nat. Rev. Cancer, 9, 108, 10.1038/nrc2544 Liu, 2017, New advances in probing cell–extracellular matrix interactions, Integr. Biol., 9, 383, 10.1039/C6IB00251J Bonnans, 2014, Remodelling the extracellular matrix in development and disease, Nat. Rev. Mol. Cell Biol., 15, 786, 10.1038/nrm3904 Alcaraz, 2004, Biomechanical approaches for studying integration of tissue structure and function in mammary epithelia, J. Mammary Gland Biol. Neoplasia, 9, 361, 10.1007/s10911-004-1406-8 Allison, 2010, Atomic force microscopy of biological samples, Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 2, 618, 10.1002/wnan.104 Acerbi, 2012, Integrin-specific mechanoresponses to compression and extension probed by cylindrical flat-ended AFM tips in lung cells, PLoS One, 7, e32261, 10.1371/journal.pone.0032261 Gimenez, 2017, Elastic properties of hydrogels and decellularized tissue sections used in mechanobiology studies probed by atomic force microscopy, Microsc. Res. Tech., 80, 85, 10.1002/jemt.22740 Jorba, 2017, Probing micromechanical properties of the extracellular matrix of soft tissues by atomic force microscopy, J. Cell. Physiol., 232, 19, 10.1002/jcp.25420 Engler, 2007, Microtissue elasticity: measurements by atomic force microscopy and its influence on cell differentiation, Methods Cell Biol., 83, 521, 10.1016/S0091-679X(07)83022-6 M. Radmacher, Studying the mechanics of cellular processes by atomic force microscopy, In: Y.L. Wang, D.E. Discher (Eds.), Cell Mechanics, 2007, pp. 347–372. Roduit, 2009, Stiffness tomography by atomic force microscopy, Biophys. J., 97, 674, 10.1016/j.bpj.2009.05.010 Kaushik, 2011, In situ mechanical analysis of myofibrillar perturbation and aging on soft, bilayered drosophila myocardium, Biophys. J., 101, 2629, 10.1016/j.bpj.2011.10.042 Radotic, 2012, Atomic force microscopy stiffness tomography on living arabidopsis thaliana cells reveals the mechanical properties of surface and deep cell-wall layers during growth, Biophys. J., 103, 386, 10.1016/j.bpj.2012.06.046 Alcaraz, 2008, Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia, EMBO J., 27, 2829, 10.1038/emboj.2008.206 Rosenbluth, 2006, Force microscopy of nonadherent cells: a comparison of leukemia cell deformability, Biophys. J ., 90, 2994, 10.1529/biophysj.105.067496 Roca-Cusachs, 2006, Rheology of passive and adhesion-activated neutrophils probed by atomic force microscopy, Biophys. J ., 91, 3508, 10.1529/biophysj.106.088831 Fernandes, 2012, Mechanical properties of epidermal cells of whole living roots of Arabidopsis thaliana: an atomic force microscopy study, Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 85, 021916, 10.1103/PhysRevE.85.021916 Gavara, 2017, A beginner's guide to atomic force microscopy probing for cell mechanics, Microsc. Res. Tech., 80, 75, 10.1002/jemt.22776 Rico, 2007, Cell dynamic adhesion and elastic properties probed with cylindrical atomic force microscopy cantilever tips, J. Mol. Recognit., 20, 459, 10.1002/jmr.829 Alcaraz, 2003, Microrheology of human lung epithelial cells measured by atomic force microscopy, Biophys. J., 84, 2071, 10.1016/S0006-3495(03)75014-0 Hübner, 2003, Downwards to metrology in nanoscale: determination of the AFM tip shape with well-known sharp-edged calibration structures, Appl. Phys. A, 76, 913, 10.1007/s00339-002-1975-6 Hutter, 1993, Calibration of atomic-force microscope tips, Rev. Sci. Instrum., 64, 1868, 10.1063/1.1143970 Gavara, 2012, Determination of the elastic moduli of thin samples and adherent cells using conical atomic force microscope tips, Nat. Nanotechnol., 7, 733, 10.1038/nnano.2012.163 Heinz, 1999, Spatially resolved force spectroscopy of biological surfaces using the atomic force microscope, Trends Biotechnol., 17, 143, 10.1016/S0167-7799(99)01304-9 Rico, 2005, Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips, Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 72, 021914, 10.1103/PhysRevE.72.021914 Alcaraz, 2002, Correction of microrheological measurements of soft samples with atomic force microscopy for the hydrodynamic drag on the cantilever, Langmuir, 18, 716, 10.1021/la0110850 Sirghi, 2006, Cleaning and hydrophilization of atomic force microscopy silicon probes, J. Phys. Chem. B, 110, 25975, 10.1021/jp063327g De Souza, 2002, Implementation of recycling routes for scanning probe microscopy tips, Microsc. Microanal., 8, 509, 10.1017/S1431927602010449 Naba, 2012, The matrisome in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices, Mol. Cell. Proteomics, 11, 10.1074/mcp.M111.014647 Sunyer, 2009, The temperature dependence of cell mechanics measured by atomic force microscopy, Phys. Biol., 6, 25009, 10.1088/1478-3975/6/2/025009 Roca-Cusachs, 2008, Micropatterning of single endothelial cell shape reveals a tight coupling between nuclear volume in G1 and proliferation, Biophys. J ., 94, 4984, 10.1529/biophysj.107.116863 Schoenenberger, 1994, Slow cellular-dynamics in mdck and r5 cells monitored by time-lapse atomic-force microscopy, Biophys. J., 67, 929, 10.1016/S0006-3495(94)80556-9 Hofmann, 1997, Investigating the cytoskeleton of chicken cardiocytes with the atomic force microscope, J. Struct. Biol., 119, 84, 10.1006/jsbi.1997.3868 A-Hassan, 1998, Relative microelastic mapping of living cells by atomic force microscopy, Biophys. J., 74, 1564, 10.1016/S0006-3495(98)77868-3 Lekka, 1999, Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy, Eur. Biophys. J. Biophys. Lett., 28, 312, 10.1007/s002490050213 Mendez, 2014, Vimentin enhances cell elastic behavior and protects against compressive stress, Biophys. J., 107, 314, 10.1016/j.bpj.2014.04.050 Charrier, 2016, Mechanical properties of intermediate filament proteins, 35 Brown, 1997, Entropic exclusion by neurofilament sidearms: a mechanism for maintaining interfilament spacing, Biochemistry, 36, 15035, 10.1021/bi9721748 Kumar, 2004, Modulation of repulsive forces between neurofilaments by sidearm phosphorylation, Biochem. Biophys. Res. Commun., 324, 489, 10.1016/j.bbrc.2004.09.076 Storm, 2005, Nonlinear elasticity in biological gels, Nature, 435, 191, 10.1038/nature03521 Kumar, 2006, Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics, Biophys. J., 90, 3762, 10.1529/biophysj.105.071506 Galgoczy, 2014, A spectrophotometer-based diffusivity assay reveals that diffusion hindrance of small molecules in extracellular matrix gels used in 3D cultures is dominated by viscous effects, Colloid Surf. B-Biointerfaces, 120, 200, 10.1016/j.colsurfb.2014.05.017 Colom, 2014, Oxygen diffusion and consumption in extracellular matrix gels: implications for designing three-dimensional cultures, J. Biomed. Mater. Res. Part A, 102, 2776, 10.1002/jbm.a.34946 Nam, 2016, Viscoplasticity enables mechanical remodeling of matrix by cells, Biophys. J., 111, 2296, 10.1016/j.bpj.2016.10.002 Mori, 2013, Transmembrane/cytoplasmic, rather than catalytic, domains of Mmp14 signal to MAPK activation and mammary branching morphogenesis via binding to integrin beta 1, Development, 140, 343, 10.1242/dev.084236 Alcaraz, 2011, Collective epithelial cell invasion overcomes mechanical barriers of collagenous extracellular matrix by a narrow tube-like geometry and MMP14-dependent local softening, Integr. Biol. (Camb.), 3, 1153, 10.1039/c1ib00073j Melo, 2014, Effects of the decellularization method on the local stiffness of acellular lungs, Tissue. Eng. Part C-Methods, 20, 412, 10.1089/ten.tec.2013.0325 Luque, 2013, Local micromechanical properties of decellularized lung scaffolds measured with atomic force microscopy, Acta Biomater., 9, 6852, 10.1016/j.actbio.2013.02.044 Uriarte, 2016, Early impairment of lung mechanics in a murine model of marfan syndrome, PLoS One, 11, 10.1371/journal.pone.0152124 Paszek, 2005, Tensional homeostasis and the malignant phenotype, Cancer Cell, 8, 241, 10.1016/j.ccr.2005.08.010 Ebihara, 2000, Changes in extracellular matrix and tissue viscoelasticity in bleomycin-induced lung fibrosis. Temporal aspects, Am. J. Respir. Crit. Care Med., 162, 1569, 10.1164/ajrccm.162.4.9912011 Perea-Gil, 2015, In vitro comparative study of two decellularization protocols in search of an optimal myocardial scaffold for recellularization, Am. J. Transl. Res., 7, 558 Andreu, 2014, Heterogeneous micromechanical properties of the extracellular matrix in healthy and infarcted hearts, Acta Biomater., 10, 3235, 10.1016/j.actbio.2014.03.034 Plodinec, 2012, The nanomechanical signature of breast cancer, Nat. Nanotechnol., 7, 757, 10.1038/nnano.2012.167 Acerbi, 2015, Human breast cancer invasion and aggression correlates with ECM stiffening and immune cell infiltration, Integr. Biol., 7, 1120, 10.1039/C5IB00040H Liu, 2010, Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression, J. Cell Biol., 190, 693, 10.1083/jcb.201004082 Engler, 2008, Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating, J. Cell Sci., 121, 3794, 10.1242/jcs.029678 Luque, 2016, Microelastic mapping of the rat dentate gyrus, R. Soc. Open Sci., 3, 7, 10.1098/rsos.150702 Nelson, 2006, Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development homeostasis, and cancer, Annu. Rev. Cell Dev. Biol., 22, 287, 10.1146/annurev.cellbio.22.010305.104315 Puig, 2015, Matrix stiffening and beta(1) integrin drive subtype-Specific fibroblast accumulation in lung cancer, Mol. Cancer Res., 13, 161, 10.1158/1541-7786.MCR-14-0155 Mitra, 2005, Focal adhesion kinase: in command and control of cell motility, Nat. Rev. Mol. Cell Biol., 6, 56, 10.1038/nrm1549 Balestrini, 2012, The mechanical memory of lung myofibroblasts, Integr. Biol., 4, 410, 10.1039/c2ib00149g Vizoso, 2015, Aberrant DNA methylation in non small cell lung cancer associated fibroblasts, Carcinogenesis, 36, 1453