Biomechanical Characterization at the Cell Scale: Present and Prospects
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
30498449
PubMed Central
PMC6249385
DOI
10.3389/fphys.2018.01449
Knihovny.cz E-zdroje
- Klíčová slova
- AFM, MEMS, cell mechanics, cell-generated forces, mechanobiology, mechanotransduction, traction force microscopy, tweezing methods,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
The rapidly growing field of mechanobiology demands for robust and reproducible characterization of cell mechanical properties. Recent achievements in understanding the mechanical regulation of cell fate largely rely on technological platforms capable of probing the mechanical response of living cells and their physico-chemical interaction with the microenvironment. Besides the established family of atomic force microscopy (AFM) based methods, other approaches include optical, magnetic, and acoustic tweezers, as well as sensing substrates that take advantage of biomaterials chemistry and microfabrication techniques. In this review, we introduce the available methods with an emphasis on the most recent advances, and we discuss the challenges associated with their implementation.
Department of Engineering Università Campus Bio Medico di Roma Rome Italy
Department of Engineering University of Cambridge Cambridge United Kingdom
Institute for Photonics and Nanotechnologies National Research Council Rome Italy
Zobrazit více v PubMed
Abidine Y., Laurent V. M., Michel R., Duperray A., Verdier C. (2015). Local mechanical properties of bladder cancer cells measured by AFM as a signature of metastatic potential. Eur. Phys. J. Plus 130:202 10.1140/epjp/i2015-15202-6 DOI
Ahmed D., Ozcelik A., Bojanala N., Nama N., Upadhyay A., Chen Y., et al. (2016). Rotational manipulation of single cells and organisms using acoustic waves. Nat. Commun. 7:11085. 10.1038/ncomms11085 PubMed DOI PMC
Alcaraz J., Otero J., Jorba I., Navajas D. (2018). Bidirectional mechanobiology between cells and their local extracellular matrix probed by atomic force microscopy. Semin. Cell Dev. Biol. 73 71–81. 10.1016/j.semcdb.2017.07.020 PubMed DOI
Andersson M., Madgavkar A., Stjerndahl M., Wu Y., Tan W., Duran R., et al. (2007). Using optical tweezers for measuring the interaction forces between human bone cells and implant surfaces: system design and force calibration. Rev. Sci. Instrum. 78:074302. 10.1063/1.2752606 PubMed DOI
Ando T. (2018). High-speed atomic force microscopy and its future prospects. Biophys. Rev. 10 285–292. 10.1007/s12551-017-0356-5 PubMed DOI PMC
Ansardamavandi A., Tafazzoli-Shadpour M., Omidvar R., Jahanzad I. (2016). Quantification of effects of cancer on elastic properties of breast tissue by atomic force microscopy. J. Mech. Behav. Biomed. Mater. 60 234–242. 10.1016/J.JMBBM.2015.12.028 PubMed DOI
Antoniolli F., Maggiolino S., Scuor N., Gallina P., Sbaizero O. (2014). A novel MEMS device for the multidirectional mechanical stimulation of single cells: preliminary results. Mech. Mach. Theory 78 131–140. 10.1016/j.mechmachtheory.2014.03.009 DOI
Ashkin A., Dziedzic J. M., Bjorkholm J. E., Chu S. (1986). Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11:288 10.1364/OL.11.000288 PubMed DOI
Ashkin A., Dziedzic J. M., Yamane T. (1987). Optical trapping and manipulation of single cells using infrared laser beams. Nature 330 769–771. 10.1038/330769a0 PubMed DOI
Balaban N. Q., Schwarz U. S., Riveline D., Goichberg P., Tzur G., Sabanay I., et al. (2001). Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3 466–472. 10.1038/35074532 PubMed DOI
Bambardekar K., Clément R., Blanc O., Chardès C., Lenne P.-F. (2015). Direct laser manipulation reveals the mechanics of cell contacts in vivo. Proc. Natl. Acad. Sci. U.S.A. 112 1416–1421. 10.1073/pnas.1418732112 PubMed DOI PMC
Bastounis E., Meili R., Álvarez-González B., Francois J., del Álamo J. C., et al. (2014). Both contractile axial and lateral traction force dynamics drive amoeboid cell motility. J. Cell Biol. 204 1045–1061. 10.1083/JCB.201307106 PubMed DOI PMC
Bausch A. R., Möller W., Sackmann E. (1999). Measurement of local viscoelasticity and forces in living cells by magnetic tweezers. Biophys. J. 76 573–579. 10.1016/S0006-3495(99)77225-5 PubMed DOI PMC
Berdyyeva T. K., Woodworth C. D., Sokolov I. (2005). Human epithelial cells increase their rigidity with ageing in vitro: direct measurements. Phys. Med. Biol. 50 81–92. 10.1088/0031-9155/50/1/007 PubMed DOI
Bergert M., Lendenmann T., Zündel M., Ehret A. E., Panozzo D., Richner P., et al. (2016). Confocal reference free traction force microscopy. Nat. Commun. 7:12814. 10.1038/ncomms12814 PubMed DOI PMC
Bidan C. M., Fratzl M., Coullomb A., Moreau P., Lombard A. H., Wang I., et al. (2018). Magneto-active substrates for local mechanical stimulation of living cells. Sci. Rep. 8:1464. 10.1038/s41598-018-19804-1 PubMed DOI PMC
Bloom R. J., George J. P., Celedon A., Sun S. X., Wirtz D. (2008). Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multiple-particle tracking. Biophys. J. 95 4077–4088. 10.1529/biophysj.108.132738 PubMed DOI PMC
Bonilla M. R., Stokes J. R., Gidley M. J., Yakubov G. E. (2015). Interpreting atomic force microscopy nanoindentation of hierarchical biological materials using multi-regime analysis. Soft Matter 11 1281–1292. 10.1039/c4sm02440k PubMed DOI
Boudou T., Legant W. R., Mu A., Borochin M. A., Thavandiran N., Radisic M., et al. (2012). A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues. Tissue Eng. Part A 18 910–919. 10.1089/ten.tea.2011.0341 PubMed DOI PMC
Bourquin Y., Syed A., Reboud J., Ranford-Cartwright L. C., Barrett M. P., Cooper J. M. (2014). Rare-cell enrichment by a rapid, label-free, ultrasonic isopycnic technique for medical diagnostics. Angew. Chemie Int. Ed. 53 5587–5590. 10.1002/anie.201310401 PubMed DOI PMC
Bronkhorst P. J., Streekstra G. J., Grimbergen J., Nijhof E. J., Sixma J. J., Brakenhoff G. J. (1995). A new method to study shape recovery of red blood cells using multiple optical trapping. Biophys. J. 69 1666–1673. 10.1016/S0006-3495(95)80084-6 PubMed DOI PMC
Butcher D. T., Alliston T., Weaver V. M. (2009). A tense situation: forcing tumour progression. Nat. Rev. Cancer 9 108–122. 10.1038/nrc2544 PubMed DOI PMC
Butler J. P., Tolić-Nørrelykke I. M., Fabry B., Fredberg J. J. (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Physiol. 282 C595–C605. 10.1152/ajpcell.00270.2001 PubMed DOI
Capitanio M., Pavone F. S. (2013). Interrogating biology with force: single molecule high-resolution measurements with optical tweezers. Biophys. J. 105 1293–1303. 10.1016/j.bpj.2013.08.007 PubMed DOI PMC
Charras G. T., Horton M. A. (2002). Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophys. J. 82 2970–2981. 10.1016/S0006-3495(02)75638-5 PubMed DOI PMC
Chen C. S., Tan J., Tien J. (2004). Mechanotransduction at cell-matrix and cell-cell contacts. Annu. Rev. Biomed. Eng. 6 275–302. 10.1146/annurev.bioeng.6.040803.140040 PubMed DOI
Chen D., Sun Y., Gudur M. S. R., Hsiao Y.-S., Wu Z., Fu J., et al. (2015). Two-bubble acoustic tweezing cytometry for biomechanical probing and stimulation of cells. Biophys. J. 108 32–42. 10.1016/j.bpj.2014.11.050 PubMed DOI PMC
Chen J., Li H., SundarRaj N., Wang J. H.-C. (2007). Alpha-smooth muscle actin expression enhances cell traction force. Cell Motil. Cytoskeleton 64 248–257. 10.1002/cm.20178 PubMed DOI
Cho Y., Park E. Y., Ko E., Park J.-S., Shin J. H. (2016). Recent advances in biological uses of traction force microscopy. Int. J. Precis. Eng. Manuf. 17 1401–1412. 10.1007/s12541-016-0166-x DOI
Ciasca G., Sassun T. E., Minelli E., Antonelli M., Papi M., Santoro A., et al. (2016). Nano-mechanical signature of brain tumours. Nanoscale 8 19629–19643. 10.1039/c6nr06840e PubMed DOI
Coceano G., Yousafzai M. S., Ma W., Ndoye F., Venturelli L., Hussain I., et al. (2016). Investigation into local cell mechanics by atomic force microscopy mapping and optical tweezer vertical indentation. Nanotechnology 27:065102. 10.1088/0957-4484/27/6/065102 PubMed DOI
Colin-York H., Fritzsche M. (2018). The future of traction force microscopy. Curr. Opin. Biomed. Eng. 5 1–5. 10.1016/J.COBME.2017.10.002 DOI
Collinsworth A. M., Zhang S., Kraus W. E., Truskey G. A. (2002). Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am. J. Physiol. Physiol. 283 C1219–C1227. 10.1152/ajpcell.00502.2001 PubMed DOI
Costa K. D., Yin F. C. (1999). Analysis of indentation: implications for measuring mechanical properties with atomic force microscopy. J. Biomech. Eng. 121 462–471. 10.1115/1.2835074 PubMed DOI
Curtis J. E., Spatz J. P. (2004). “Getting a grip: hyaluronan-mediated cellular adhesion,” in Proceedings of the International Society for Optics and Photonics, eds Dholakia K., Spalding G. C. (Washington, DC: SPIE; ), 455–466. 10.1117/12.560049 DOI
De Vlaminck I., Dekker C. (2012). Recent advances in magnetic tweezers. Annu. Rev. Biophys. 41 453–472. 10.1146/annurev-biophys-122311-100544 PubMed DOI
Del Alamo J. C., Meili R., Alonso-Latorre B., Rodríguez-Rodríguez J., Aliseda A., Firtel R. A., et al. (2007). Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry. Proc. Natl. Acad. Sci. U.S.A. 104 13343–13348. 10.1073/pnas.0705815104 PubMed DOI PMC
Dholakia K., Reece P. (2006). Optical micromanipulation takes hold. Nano Today 1 18–27. 10.1016/S1748-0132(06)70019-6 PubMed DOI
Digiuni S., Berne-Dedieu A., Martinez-Torres C., Szecsi J., Bendahmane M., Arneodo A., et al. (2015). Single cell wall nonlinear mechanics revealed by a multiscale analysis of AFM force-indentation curves. Biophys. J. 1082235–2248. 10.1016/j.bpj.2015.02.024 PubMed DOI PMC
Ding X., Li P., Lin S.-C. S., Stratton Z. S., Nama N., Guo F., et al. (2013). Surface acoustic wave microfluidics. Lab Chip 13 3626–3649. 10.1039/c3lc50361e PubMed DOI PMC
Ding X., Peng Z., Lin S.-C. S., Geri M., Li S., Li P., et al. (2014). Cell separation using tilted-angle standing surface acoustic waves. Proc. Natl. Acad. Sci. U.S.A. 111 12992–12997. 10.1073/pnas.1413325111 PubMed DOI PMC
Dinu C. Z., Dong C., Hu X. (2016). Current status and perspectives in atomic force microscopy-based identification of cellular transformation. Int. J. Nanomedicine 11 2107–2018. 10.2147/IJN.S103501 PubMed DOI PMC
du Roure O., Saez A., Buguin A., Austin R. H., Chavrier P., Silberzan P., et al. (2005). Force mapping in epithelial cell migration. Proc. Natl. Acad. Sci. U.S.A. 102 2390–2395. 10.1073/pnas.0408482102 PubMed DOI PMC
Dufrêne Y. F., Pelling A. E. (2013). Force nanoscopy of cell mechanics and cell adhesion. Nanoscale 5:4094. 10.1039/c3nr00340j PubMed DOI
Dulińska I., Targosz M., Strojny W., Lekka M., Czuba P., Balwierz W., et al. (2006). Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. J. Biochem. Biophys. Methods 66 1–11. 10.1016/j.jbbm.2005.11.003 PubMed DOI
Efremov Y. M., Dokrunova A. A., Efremenko A. V., Kirpichnikov M. P., Shaitan K. V., Sokolova O. S. (2015). Distinct impact of targeted actin cytoskeleton reorganization on mechanical properties of normal and malignant cells. Biochim. Biophys. Acta Mol. Cell Res. 1853 3117–3125. 10.1016/j.bbamcr.2015.05.008 PubMed DOI
El-Kirat-Chatel S., Dufrêne Y. F. (2012). Nanoscale imaging of the Candida –macrophage interaction using correlated fluorescence-atomic force microscopy. ACS Nano 6 10792–10799. 10.1021/nn304116f PubMed DOI
Engler A. J., Sen S., Sweeney H. L., Discher D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126 677–689. 10.1016/j.cell.2006.06.044 PubMed DOI
Fabry B., Maksym G. N., Butler J. P., Glogauer M., Navajas D., Fredberg J. J. (2001). Scaling the microrheology of living cells. Phys. Rev. Lett. 87:148102. 10.1103/PhysRevLett.87.148102 PubMed DOI
Fallqvist B., Fielden M. L., Pettersson T., Nordgren N., Kroon M., Gad A. K. B. (2016). Experimental and computational assessment of F-actin influence in regulating cellular stiffness and relaxation behaviour of fibroblasts. J. Mech. Behav. Biomed. Mater. 59 168–184. 10.1016/j.jmbbm.2015.11.039 PubMed DOI
Fan Z., Sun Y., Di C., Tay D., Chen W., Deng C. X., et al. (2013). Acoustic tweezing cytometry for live-cell subcellular modulation of intracellular cytoskeleton contractility. Sci. Rep. 3:2176. 10.1038/srep02176 PubMed DOI PMC
Fazal F. M., Block S. M. (2011). Optical tweezers study life under tension. Nat. Photonics 5 318–321. 10.1038/nphoton.2011.100 PubMed DOI PMC
Finer J. T., Simmons R. M., Spudich J. A. (1994). Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368 113–119. 10.1038/368113a0 PubMed DOI
Fior R., Maggiolino S., Codan B., Lazzarino M., Sbaizero O. (2011). “A study on the cellular structure during stress solicitation induced by BioMEMS,” in Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, (Boston, MA: IEEE), 2455–2458. 10.1109/IEMBS.2011.6090682 PubMed DOI
Foo J.-J., Liu K.-K., Chan V. (2003). Thermal effect on a viscously deformed liposome in a laser trap. Ann. Biomed. Eng. 31 354–362. 10.1114/1.1555626 PubMed DOI
Foo J. J., Liu K. K., Chan V. (2004). Viscous drag of deformed vesicles in optical trap: Experiments and simulations. AIChE J. 50 249–254. 10.1002/aic.10023 DOI
Formosa-Dague C., Duval R. E., Dague E. (2018). Cell biology of microbes and pharmacology of antimicrobial drugs explored by atomic force microscopy. Semin. Cell Dev. Biol. 73 165–176. 10.1016/j.semcdb.2017.06.022 PubMed DOI
Franck C., Maskarinec S. A., Tirrell D. A., Ravichandran G. (2011). Three-dimensional traction force microscopy: a new tool for quantifying cell-matrix interactions. PLoS One 6:e17833. 10.1371/journal.pone.0017833 PubMed DOI PMC
Friend J., Yeo L. Y. (2011). Microscale acoustofluidics: microfluidics driven via acoustics and ultrasonics. Rev. Mod. Phys. 83 647–704. 10.1103/RevModPhys.83.647 DOI
Fu J., Wang Y.-K., Yang M. T., Desai R. A., Yu X., Liu Z., et al. (2010). Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Methods 7 733–736. 10.1038/nmeth.1487 PubMed DOI PMC
Fuhrer R., Schumacher C. M., Zeltner M., Stark W. J. (2013). Soft iron/silicon composite tubes for magnetic peristaltic pumping: frequency-dependent pressure and volume flow. Adv. Funct. Mater. 23 3845–3849. 10.1002/adfm.201203572 DOI
Galbraith C. G., Sheetz M. P. (1998). Forces on adhesive contacts affect cell function. Curr. Opin. Cell Biol. 10 566–571. 10.1016/S0955-0674(98)80030-6 PubMed DOI
Galbraith C. G., Yamada K. M., Sheetz M. P. (2002). The relationship between force and focal complex development. J. Cell Biol. 159 695–705. 10.1083/jcb.200204153 PubMed DOI PMC
Gautier H. O. B., Thompson A. J., Achouri S., Koser D. E., Holtzmann K., Moeendarbary E., et al. (2015). Atomic force microscopy-based force measurements on animal cells and tissues. Methods Cell Biol. 125 211–235. 10.1016/BS.MCB.2014.10.005 PubMed DOI
Gavara N., Roca-Cusachs P., Sunyer R., Farré R., Navajas D. (2008). Mapping cell-matrix stresses during stretch reveals inelastic reorganization of the cytoskeleton. Biophys. J. 95 464–471. 10.1529/biophysj.107.124180 PubMed DOI PMC
Geiger B., Bershadsky A. (2001). Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13 584–592. 10.1016/S0955-0674(00)00255-6 PubMed DOI
Gesellchen F., Bernassau A. L., Déjardin T., Cumming D. R. S., Riehle M. O. (2014). Cell patterning with a heptagon acoustic tweezer – application in neurite guidance. Lab Chip 14 2266–2275. 10.1039/C4LC00436A PubMed DOI
Ghassemi S., Meacci G., Liu S., Gondarenko A. A., Mathur A., Roca-Cusachs P., et al. (2012). Cells test substrate rigidity by local contractions on submicrometer pillars. Proc. Natl. Acad. Sci. U.S.A. 109 5328–5333. 10.1073/pnas.1119886109 PubMed DOI PMC
Ghibaudo M., Saez A., Trichet L., Xayaphoummine A., Browaeys J., Silberzan P., et al. (2008). Traction forces and rigidity sensing regulate cell functions. Soft Matter 4 1836–1843. 10.1039/b804103b PubMed DOI
Glogauer M., Arora P., Yao G., Sokholov I., Ferrier J., McCulloch C. A. (1997). Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J. Cell Sci. 110(Pt 1), 11–21. PubMed
Glogauer M., Ferrier J., McCulloch C. A. (1995). Magnetic fields applied to collagen-coated ferric oxide beads induce stretch-activated Ca2 + flux in fibroblasts. Am. J. Physiol. 269(5 Pt 1), C1093–C1104. 10.1152/ajpcell.1995.269.5.C1093 PubMed DOI
Gosse C., Croquette V. (2002). Magnetic tweezers: micromanipulation and force measurement at the molecular level. Biophys. J. 82 3314–3329. 10.1016/S0006-3495(02)75672-5 PubMed DOI PMC
Grady M. E., Composto R. J., Eckmann D. M. (2016). Cell elasticity with altered cytoskeletal architectures across multiple cell types. J. Mech. Behav. Biomed. Mater. 61 197–207. 10.1016/j.jmbbm.2016.01.022 PubMed DOI
Grier D. G. (2003). A revolution in optical manipulation. Nature 424 810–816. 10.1038/nature01935 PubMed DOI
Gu M., Kuriakose S., Gan X. (2007). A single beam near-field laser trap for optical stretching, folding and rotation of erythrocytes. Opt. Express 15:1369. 10.1364/OE.15.001369 PubMed DOI
Guck J., Ananthakrishnan R., Mahmood H., Moon T. J., Cunningham C. C., Käs J. (2001). The optical stretcher: a novel laser tool to micromanipulate cells. Biophys. J. 81 767–784. 10.1016/S0006-3495(01)75740-2 PubMed DOI PMC
Guck J., Schinkinger S., Lincoln B., Wottawah F., Ebert S., Romeyke M., et al. (2005). Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 88 3689–3698. 10.1529/biophysj.104.045476 PubMed DOI PMC
Guo F., Li P., French J. B., Mao Z., Zhao H., Li S., et al. (2015). Controlling cell-cell interactions using surface acoustic waves. Proc. Natl. Acad. Sci. U.S.A. 112 43–48. 10.1073/pnas.1422068112 PubMed DOI PMC
Guo F., Mao Z., Chen Y., Xie Z., Lata J. P., Li P., et al. (2016). Three-dimensional manipulation of single cells using surface acoustic waves. Proc. Natl. Acad. Sci. U.S.A. 113 1522–1527. 10.1073/pnas.1524813113 PubMed DOI PMC
Guolla L., Bertrand M., Haase K., Pelling A. E. (2012). Force transduction and strain dynamics in actin stress fibres in response to nanonewton forces. J. Cell Sci. 125 603–613. 10.1242/jcs.088302 PubMed DOI
Gupta M., Kocgozlu L., Sarangi B. R., Margadant F., Ashraf M., Ladoux B. (2015). Micropillar substrates: a tool for studying cell mechanobiology. Biophys. Methods Cell Biol. 125 289–308. 10.1016/bs.mcb.2014.10.009 PubMed DOI
Hall M., Long R., Feng X., Huang Y., Hui C. Y., Wu M. (2013). Toward single cell traction microscopy within 3D collagen matrices. Exp. Cell Res. 319 2396–2408. 10.1016/j.yexcr.2013.06.009 PubMed DOI PMC
Han Y., Wang J., Wang K., Dong S. (2016). Fabrication of atomic force microscope spherical tips and its application in determining the mechanical property of cancer cells. Micro Nano Lett. 11 881–884. 10.1049/mnl.2016.0319 DOI
Harlepp S., Thalmann F., Follain G., Goetz J. G. (2017). Hemodynamic forces can be accurately measured in vivo with optical tweezers. Mol. Biol. Cell 28 3252–3260. 10.1091/mbc.E17-06-0382 PubMed DOI PMC
Harris A. K., Wild P., Stopak D. (1980). Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208 177–179. 10.1126/science.6987736 PubMed DOI
Harris A. R., Charras G. T. (2011). Experimental validation of atomic force microscopy-based cell elasticity measurements. Nanotechnology 22:345102. 10.1088/0957-4484/22/34/345102 PubMed DOI
Håti A. G., Aachmann F. L., Stokke B. T., Skjåk-Brk G., Sletmoen M. (2015). Energy landscape of alginate-epimerase interactions assessed by optical tweezers and atomic force microscopy. PLoS One 10:e0141237. 10.1371/journal.pone.0141237 PubMed DOI PMC
Haupt B. J., Pelling A. E., Horton M. A. (2006). Integrated confocal and scanning probe microscopy for biomedical research. ScientificWorldJournal 6 1609–1618. 10.1100/tsw.2006.269 PubMed DOI PMC
Hayashi K., Higaki M. (2017). Stiffness of intact endothelial cells from fresh aortic bifurcations of atherosclerotic rabbits-atomic force microscopic study. J. Cell. Physiol. 232 7–13. 10.1002/jcp.25379 PubMed DOI
Hendricks A. G., Holzbaur E. L. F., Goldman Y. E. (2012). Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors. Proc. Natl. Acad. Sci. U.S.A. 109 18447–18452. 10.1073/pnas.1215462109 PubMed DOI PMC
Hénon S., Lenormand G., Richert A., Gallet F. (1999). A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys. J. 76 1145–1151. 10.1016/S0006-3495(99)77279-6 PubMed DOI PMC
Hertz H. (1896). Ueber die Berührung fester elastischer Körper. J. für die reine und Angew. Math. 92 156–171.
Heureaux J., Chen D., Murray V. L., Deng C. X., Liu A. P. (2014). Activation of a bacterial mechanosensitive channel in mammalian cells by cytoskeletal stress. Cell. Mol. Bioeng. 7 307–319. 10.1007/s12195-014-0337-8 PubMed DOI PMC
Hinson J. T., Chopra A., Nafissi N., Polacheck W. J., Benson C. C., Swist S., et al. (2015). HEART DISEASE. Titin mutations in iPS cells define sarcomere insufficiency as a cause of dilated cardiomyopathy. Science 349 982–986. 10.1126/science.aaa5458 PubMed DOI PMC
Hinterdorfer P., Dufrêne Y. F. (2006). Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods 3 347–355. 10.1038/nmeth871 PubMed DOI
Hoffman B. D., Grashoff C., Schwartz M. A. (2011). Dynamic molecular processes mediate cellular mechanotransduction. Nature 475 316–323. 10.1038/nature10316 PubMed DOI PMC
Hu S., Eberhard L., Chen J., Love J. C., Butler J. P., Fredberg J. J., et al. (2004). Mechanical anisotropy of adherent cells probed by a three-dimensional magnetic twisting device. Am. J. Physiol. 287 C1184–C1191. 10.1152/ajpcell.00224.2004 PubMed DOI
Huang P.-H., Chan C. Y., Li P., Nama N., Xie Y., Wei C.-H., et al. (2015). A spatiotemporally controllable chemical gradient generator via acoustically oscillating sharp-edge structures. Lab Chip 15 4166–4176. 10.1039/c5lc00868a PubMed DOI PMC
Huang S., Ingber D. E. (1999). The structural and mechanical complexity of cell-growth control. Nat. Cell Biol. 1 E131–E138. 10.1038/13043 PubMed DOI
Huang W., Anvari B., Torres J. H., Lebaron R. G., Athanasiou K. A. (2003). Temporal effects of cell adhesion on mechanical characteristics of the single chondrocyte. J. Orthop. Res. 21 88–95. 10.1016/S0736-0266(02)00130-4 PubMed DOI
Hwang J. Y., Lim H. G., Yoon C. W., Lam K. H., Yoon S., Lee C., et al. (2014). Non-contact high-frequency ultrasound microbeam stimulation for studying mechanotransduction in human umbilical vein endothelial cells. Ultrasound Med. Biol. 40 2172–2182. 10.1016/j.ultrasmedbio.2014.03.018 PubMed DOI PMC
Ichikawa M., Yoshikawa K. (2001). Optical transport of a single cell-sized liposome. Appl. Phys. Lett. 79 4598–4600. 10.1063/1.1430026 DOI
Indra I., Undyala V., Kandow C., Thirumurthi U., Dembo M., Beningo K. A. (2011). An in vitro correlation of mechanical forces and metastatic capacity. Phys. Biol. 8:015015. 10.1088/1478-3975/8/1/015015 PubMed DOI PMC
Jannat R. A., Dembo M., Hammer D. A. (2011). Traction forces of neutrophils migrating on compliant substrates. Biophys. J. 101 575–584. 10.1016/j.bpj.2011.05.040 PubMed DOI PMC
Janssen X. J. A., Lipfert J., Jager T., Daudey R., Beekman J., Dekker N. H. (2012). Electromagnetic torque tweezers: a versatile approach for measurement of single-molecule twist and torque. Nano Lett. 12 3634–3639. 10.1021/nl301330h PubMed DOI
Johansen P. L., Fenaroli F., Evensen L., Griffiths G., Koster G. (2016). Optical micromanipulation of nanoparticles and cells inside living zebrafish. Nat. Commun. 7:10974. 10.1038/ncomms10974 PubMed DOI PMC
Karácsony O., Akhremitchev B. B. (2011). On the detection of single bond ruptures in dynamic force spectroscopy by AFM. Langmuir 27 11287–11291. 10.1021/la202530j PubMed DOI
Kasas S., Gmur T., Dietler G. (2017). “Finite-element analysis of microbiological structures,” in The World of Nano-Biomechanics, ed. Ikai A. (Amsterdam: Elsevier; ), 199–218. 10.1016/B978-0-444-63686-7.00011-0 DOI
Kasas S., Stupar P., Dietler G. (2018). AFM contribution to unveil pro- and eukaryotic cell mechanical properties. Semin. Cell Dev. Biol. 73 177–187. 10.1016/j.semcdb.2017.08.032 PubMed DOI
Khetan S., Guvendiren M., Legant W. R., Cohen D. M., Chen C. S., Burdick J. A. (2013). Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat. Mater. 12 458–465. 10.1038/nmat3586 PubMed DOI PMC
Kilinc D., Blasiak A., O’Mahony J. J., Suter D. M., Lee G. U. (2012). Magnetic tweezers-based force clamp reveals mechanically distinct apCAM domain interactions. Biophys. J. 103 1120–1129. 10.1016/j.bpj.2012.08.025 PubMed DOI PMC
Kilinc D., Lee G. U. (2014). Advances in magnetic tweezers for single molecule and cell biophysics. Integr. Biol. 6 27–34. 10.1039/c3ib40185e PubMed DOI
Kim D.-H., Wong P. K., Park J., Levchenko A., Sun Y. (2009). Microengineered platforms for cell mechanobiology. Annu. Rev. Biomed. Eng. 11 203–233. 10.1146/annurev-bioeng-061008-124915 PubMed DOI
Kis A., Kasas S., Babić B., Kulik A. J., Benoît W., Briggs G. A. D., et al. (2002). Nanomechanics of microtubules. Phys. Rev. Lett. 89:248101. 10.1103/PhysRevLett.89.248101 PubMed DOI
Knöner G., Rolfe B. E., Campbell J. H., Parkin S. J., Heckenberg N. R., Rubinsztein-Dunlop H. (2006). Mechanics of cellular adhesion to artificial artery templates. Biophys. J. 91 3085–3096. 10.1529/biophysj.105.076125 PubMed DOI PMC
Koch T. M., Münster S., Bonakdar N., Butler J. P., Fabry B. (2012). 3D traction forces in cancer cell invasion. PLoS One 7:e33476. 10.1371/journal.pone.0033476 PubMed DOI PMC
Kodera N., Yamamoto D., Ishikawa R., Ando T. (2010). Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468 72–76. 10.1038/nature09450 PubMed DOI
Kuznetsova T. G., Starodubtseva M. N., Yegorenkov N. I., Chizhik S. A., Zhdanov R. I. (2007). Atomic force microscopy probing of cell elasticity. Micron 38 824–833. 10.1016/J.MICRON.2007.06.011 PubMed DOI
Lam K. H., Li Y., Li Y., Lim H. G., Zhou Q., Shung K. K. (2016). Multifunctional single beam acoustic tweezer for non-invasive cell/organism manipulation and tissue imaging. Sci. Rep. 6:37554. 10.1038/srep37554 PubMed DOI PMC
Lam R. H. W., Sun Y., Chen W., Fu J. (2012a). Elastomeric microposts integrated into microfluidics for flow-mediated endothelial mechanotransduction analysis. Lab Chip 12 1865–1873. 10.1039/c2lc21146g PubMed DOI PMC
Lam R. H. W., Weng S., Lu W., Fu J. (2012b). Live-cell subcellular measurement of cell stiffness using a microengineered stretchable micropost array membrane. Integr. Biol. 4 1289–1298. 10.1039/c2ib20134h PubMed DOI PMC
Lam W. A., Chaudhuri O., Crow A., Webster K. D., Li T.-D., Kita A., et al. (2011). Mechanics and contraction dynamics of single platelets and implications for clot stiffening. Nat. Mater. 10 61–66. 10.1038/nmat2903 PubMed DOI PMC
Lee J., Leonard M., Oliver T., Ishihara A., Jacobson K. (1994). Traction forces generated by locomoting keratocytes. J. Cell Biol. 127 1957–1964. 10.1083/jcb.127.6.1957 PubMed DOI PMC
Legant W. R., Miller J. S., Blakely B. L., Cohen D. M., Genin G. M., Chen C. S. (2010). Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat. Methods 7 969–971. 10.1038/nmeth.1531 PubMed DOI PMC
Lehenkari P. P., Charras G. T., Nykänen A., Horton M. A. (2000). Adapting atomic force microscopy for cell biology. Ultramicroscopy 82 289–295. 10.1016/S0304-3991(99)00138-2 PubMed DOI
Lekka M. (2016). Discrimination between normal and cancerous cells using AFM. Bionanoscience 6 65–80. 10.1007/s12668-016-0191-3 PubMed DOI PMC
Li B., Li F., Puskar K. M., Wang J. H.-C. (2009). Spatial patterning of cell proliferation and differentiation depends on mechanical stress magnitude. J. Biomech. 42 1622–1627. 10.1016/j.jbiomech.2009.04.033 PubMed DOI PMC
Li B., Lin M., Tang Y., Wang B., Wang J. H.-C. (2008). A novel functional assessment of the differentiation of micropatterned muscle cells. J. Biomech. 41 3349–3353. 10.1016/j.jbiomech.2008.09.025 PubMed DOI PMC
Li B., Wang J. H.-C. (2011). Fibroblasts and myofibroblasts in wound healing: Force generation and measurement. J. Tissue Viability 20 108–120. 10.1016/j.jtv.2009.11.004 PubMed DOI PMC
Li B., Xie L., Starr Z. C., Yang Z., Lin J.-S., Wang J. H.-C. (2007). Development of micropost force sensor array with culture experiments for determination of cell traction forces. Cell Motil. Cytoskeleton 64 509–518. 10.1002/cm.20200 PubMed DOI
Li P., Mao Z., Peng Z., Zhou L., Chen Y., Huang P.-H., et al. (2015). Acoustic separation of circulating tumor cells. Proc. Natl. Acad. Sci. U.S.A. 112 4970–4975. 10.1073/pnas.1504484112 PubMed DOI PMC
Lieber S. C., Aubry N., Pain J., Diaz G., Kim S. J., Vatner S. F. (2004). Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. Am. J. Physiol. Heart Circ. Phisiol. 287 H645–H651. 10.1152/ajpheart.00564.2003 PubMed DOI
Lim C. T., Dao M., Suresh S., Sow C. H., Chew K. T. (2004). Large deformation of living cells using laser traps. Acta Mater. 52 1837–1845. 10.1016/J.ACTAMAT.2003.12.028 DOI
Lin I.-K., Liao Y.-M., Liu Y., Ou K.-S., Chen K.-S., Zhang X. (2008). Viscoelastic mechanical behavior of soft microcantilever-based force sensors. Appl. Phys. Lett. 93 251907 10.1063/1.3056114 DOI
Lin Y.-C., Kramer C. M., Chen C. S., Reich D. H. (2012). Probing cellular traction forces with magnetic nanowires and microfabricated force sensor arrays. Nanotechnology 23:075101. 10.1088/0957-4484/23/7/075101 PubMed DOI PMC
Lipfert J., Kerssemakers J. W. J., Jager T., Dekker N. H. (2010). Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA-DNA filaments. Nat. Methods 7 977–980. 10.1038/nmeth.1520 PubMed DOI
Lipfert J., Wiggin M., Kerssemakers J. W. J., Pedaci F., Dekker N. H. (2011). Freely orbiting magnetic tweezers to directly monitor changes in the twist of nucleic acids. Nat. Commun. 2:439. 10.1038/ncomms1450 PubMed DOI PMC
Lisica A., Grill S. W. (2017). Optical tweezers studies of transcription by eukaryotic RNA polymerases. Biomol. Concepts 8 1–11. 10.1515/bmc-2016-0028 PubMed DOI
Liu A. P. (2016). Biophysical tools for cellular and subcellular mechanical actuation of cell signaling. Biophys. J. 111 1112–1118. 10.1016/J.BPJ.2016.02.043 PubMed DOI PMC
Liu J., Sun N., Bruce M. A., Wu J. C., Butte M. J. (2012). Atomic force mechanobiology of pluripotent stem cell-derived cardiomyocytes. PLoS One 7:e37559. 10.1371/journal.pone.0037559 PubMed DOI PMC
López-Quesada C., Fontaine A.-S., Farré A., Joseph M., Selva J., Egea G., et al. (2014). Artificially-induced organelles are optimal targets for optical trapping experiments in living cells. Biomed. Opt. Express 5:1993. 10.1364/BOE.5.001993 PubMed DOI PMC
Mahaffy R. E., Park S., Gerde E., Käs J., Shih C. K. (2004). Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy. Biophys. J. 86 1777–1793. 10.1016/S0006-3495(04)74245-9 PubMed DOI PMC
Malandrino A., Kamm R. D., Moeendarbary E. (2018). In vitro modeling of mechanics in cancer metastasis. ACS Biomater. Sci. Eng. 4 294–301. 10.1021/acsbiomaterials.7b00041 PubMed DOI PMC
Maloney J. M., Nikova D., Lautenschläger F., Clarke E., Langer R., Guck J., et al. (2010). Mesenchymal stem cell mechanics from the attached to the suspended state. Biophys. J. 99 2479–2487. 10.1016/j.bpj.2010.08.052 PubMed DOI PMC
Mammoto T., Ingber D. E. (2010). Mechanical control of tissue and organ development. Development 137 1407–1420. 10.1242/dev.024166 PubMed DOI PMC
Mann J. M., Lam R. H. W., Weng S., Sun Y., Fu J. (2012). A silicone-based stretchable micropost array membrane for monitoring live-cell subcellular cytoskeletal response. Lab Chip 12 731–740. 10.1039/C2LC20896B PubMed DOI PMC
Marjoram R. J., Guilluy C., Burridge K. (2016). Using magnets and magnetic beads to dissect signaling pathways activated by mechanical tension applied to cells. Methods 94 19–26. 10.1016/j.ymeth.2015.09.025 PubMed DOI PMC
Martinez-Martin D., Carrasco C., Hernando-Perez M., de Pablo P. J., Gomez-Herrero J., Perez R., et al. (2012). Resolving structure and mechanical properties at the nanoscale of viruses with frequency modulation atomic force microscopy. PLoS One 7:e30204. 10.1371/journal.pone.0030204 PubMed DOI PMC
Mathur A. B., Truskey G. A., Reichert W. M. (2000). Atomic force and total internal reflection fluorescence microscopy for the study of force transmission in endothelial cells. Biophys. J. 78 1725–1735. 10.1016/S0006-3495(00)76724-5 PubMed DOI PMC
Matsudaira K., Nguyen T.-V., Shoji K. H., Tsukagoshi T., Takahata T., Shimoyama I. (2017). MEMS piezoresistive cantilever for the direct measurement of cardiomyocyte contractile force. J. Micromech. Microeng. 27:105005 10.1088/1361-6439/aa8350 DOI
Matthews B. D. (2006). Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J. Cell Sci. 119 508–518. 10.1242/jcs.02760 PubMed DOI
Maugeri-Saccà M., De Maria R. (2018). The Hippo pathway in normal development and cancer. Pharmacol. Ther. 10.1016/J.PHARMTHERA.2017.12.011 PubMed DOI
Mercadé-Prieto R., Thomas C. R., Zhang Z. (2013). Mechanical double layer model for Saccharomyces Cerevisiae cell wall. Eur. Biophys. J. 42 613–620. 10.1007/s00249-013-0909-x PubMed DOI
Miroshnikova Y. A., Le H. Q., Schneider D., Thalheim T., Rübsam M., Bremicker N., et al. (2018). Adhesion forces and cortical tension couple cell proliferation and differentiation to drive epidermal stratification. Nat. Cell Biol. 20 69–80. 10.1038/s41556-017-0005-z PubMed DOI
Monachino E., Spenkelink L. M., van Oijen A. M. (2017). Watching cellular machinery in action, one molecule at a time. J. Cell Biol. 216 41–51. 10.1083/jcb.201610025 PubMed DOI PMC
Morton K. C., Baker L. A. (2014). Atomic force microscopy-based bioanalysis for the study of disease. Anal. Methods 6 4932–4955. 10.1039/C4AY00485J DOI
Mosconi F., Allemand J. F., Croquette V. (2011). Soft magnetic tweezers: a proof of principle. Rev. Sci. Instrum. 82:034302. 10.1063/1.3531959 PubMed DOI
Moulding D. A., Moeendarbary E., Valon L., Record J., Charras G. T., Thrasher A. J. (2012). Excess F-actin mechanically impedes mitosis leading to cytokinesis failure in X-linked neutropenia by exceeding Aurora B kinase error correction capacity. Blood 120 3803–3811. 10.1182/blood-2012-03-419663 PubMed DOI PMC
Mukherjee R., Saha M., Routray A., Chakraborty C. (2015). Nanoscale surface characterization of human erythrocytes by atomic force microscopy: a critical review. IEEE Trans. Nanobioscience 14 625–633. 10.1109/TNB.2015.2424674 PubMed DOI
Munoz J. J. (2016). Non-regularised inverse finite element analysis for 3D traction force microscopy. Int. J. Numer. Anal. Model. 13 763–781.
Na S., Wang N. (2008). Application of fluorescence resonance energy transfer and magnetic twisting cytometry to quantify mechanochemical signaling activities in a living cell. Sci. Signal. 1:pl1. 10.1126/scisignal.134pl1 PubMed DOI PMC
Nan X., Sims P. A., Xie X. S. (2008). Organelle tracking in a living cell with microsecond time resolution and nanometer spatial precision. ChemPhysChem 9 707–712. 10.1002/cphc.200700839 PubMed DOI
Nardone G., Oliver-De, La Cruz J., Vrbsky J., Martini C., Pribyl J., et al. (2017). YAP regulates cell mechanics by controlling focal adhesion assembly. Nat. Commun. 8:15321. 10.1038/ncomms15321 PubMed DOI PMC
Nelson C. M., Jean R. P., Tan J. L., Liu W. F., Sniadecki N. J., Spector A. A., et al. (2005). Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. U.S.A. 102 11594–11599. 10.1073/pnas.0502575102 PubMed DOI PMC
Neuman K. C., Chadd E. H., Liou G. F., Bergman K., Block S. M. (1999). Characterization of photodamage to Escherichia coli in optical traps. Biophys. J. 77 2856–2863. 10.1016/S0006-3495(99)77117-1 PubMed DOI PMC
Nguyen V., Kaulen C., Simon U., Schnakenberg U. (2017). Single interdigital transducer approach for gravimetrical SAW sensor applications in liquid environments. Sensors 17:2931. 10.3390/s17122931 PubMed DOI PMC
Norman J. J., Mukundan V., Bernstein D., Pruitt B. L. (2008). Microsystems for biomechanical measurements. Pediatr. Res. 63 576–583. 10.1203/PDR.0b013e31816b2ec4 PubMed DOI
Oberstrass F. C., Fernandes L. E., Bryant Z. (2012). Torque measurements reveal sequence-specific cooperative transitions in supercoiled DNA. Proc. Natl. Acad. Sci. U.S.A. 109 6106–6111. 10.1073/pnas.1113532109 PubMed DOI PMC
Oddershede L. B. (2012). Force probing of individual molecules inside the living cell is now a reality. Nat. Chem. Biol. 8 879–886. 10.1038/nchembio.1082 PubMed DOI
O’Mahony J. J., Platt M., Kilinc D., Lee G. (2013). Synthesis of superparamagnetic particles with tunable morphologies: the role of nanoparticle–nanoparticle interactions. Langmuir 29 2546–2553. 10.1021/la3047565 PubMed DOI
Pal S. (ed.). (2014). “Mechanical properties of biological materials,” in Design of Artificial Human Joints & Organs (Boston, MA: Springer; ), 23–40. 10.1007/978-1-4614-6255-2_2 DOI
Palacio J., Jorge-Peñas A., Muñoz-Barrutia A., Ortiz-de-Solorzano C., de Juan-Pardo E., García-Aznar J. M. (2013). Numerical estimation of 3D mechanical forces exerted by cells on non-linear materials. J. Biomech. 46 50–55. 10.1016/j.jbiomech.2012.10.009 PubMed DOI
Park J., Ryu J., Choi S. K., Seo E., Cha J. M., Ryu S., et al. (2005). Real-time measurement of the contractile forces of self-organized cardiomyocytes on hybrid biopolymer microcantilevers. Anal. Chem. 77 6571–6580. 10.1021/ac0507800 PubMed DOI
Park S., Jang W.-J., Jeong C.-H. (2016). Nano-biomechanical validation of epithelial–mesenchymal transition in oral squamous cell carcinomas. Biol. Pharm. Bull. 39 1488–1495. 10.1248/bpb.b16-00266 PubMed DOI
Park Y., Best C. A., Badizadegan K., Dasari R. R., Feld M. S., Kuriabova T., et al. (2010). Measurement of red blood cell mechanics during morphological changes. Proc. Natl. Acad. Sci. U.S.A. 107 6731–6736. 10.1073/pnas.0909533107 PubMed DOI PMC
Pesen D., Hoh J. H. (2005). Micromechanical architecture of the endothelial cell cortex. Biophys. J. 88 670–679. 10.1529/BIOPHYSJ.104.049965 PubMed DOI PMC
Plodinec M., Loparic M., Monnier C. A., Obermann E. C., Zanetti-Dallenbach R., Oertle P., et al. (2012). The nanomechanical signature of breast cancer. Nat. Nanotechnol. 7 757–765. 10.1038/nnano.2012.167 PubMed DOI
Poh Y.-C., Na S., Chowdhury F., Ouyang M., Wang Y., Wang N. (2009). Rapid activation of Rac GTPase in living cells by force is independent of Src. PLoS One 4:e7886. 10.1371/journal.pone.0007886 PubMed DOI PMC
Polacheck W. J., Chen C. S. (2016). Measuring cell-generated forces: a guide to the available tools. Nat. Methods 13 415–423. 10.1038/nmeth.3834 PubMed DOI PMC
Polacheck W. J., Li R., Uzel S. G. M., Kamm R. D. (2013). Microfluidic platforms for mechanobiology. Lab Chip 13 2252–2267. 10.1039/c3lc41393d PubMed DOI PMC
Puchner E. M., Gaub H. E. (2009). Force and function: probing proteins with AFM-based force spectroscopy. Curr. Opin. Struct. Biol. 19 605–614. 10.1016/J.SBI.2009.09.005 PubMed DOI
Puig-de-Morales M., Millet E., Fabry B., Navajas D., Wang N., Butler J. P., et al. (2004). Cytoskeletal mechanics in adherent human airway smooth muscle cells: probe specificity and scaling of protein-protein dynamics. Am. J. Physiol. Physiol. 287 C643–C654. 10.1152/ajpcell.00070.2004 PubMed DOI
Rajagopalan J., Saif M. T. A. (2011). MEMS sensors and microsystems for cell mechanobiology. J. Micromech. Microeng. 21:054002. 10.1088/0960-1317/21/5/054002 PubMed DOI PMC
Rianna C., Radmacher M. (2016). “Cell mechanics as a marker for diseases: Biomedical applications of AFM,” in Proceedings of the AIP Conference Proceedings (Melville, NY: AIP Publishing LLC; ), 020057 10.1063/1.4960276. DOI
Ricart B. G., Yang M. T., Hunter C. A., Chen C. S., Hammer D. A. (2011). Measuring traction forces of motile dendritic cells on micropost arrays. Biophys. J. 101 2620–2628. 10.1016/j.bpj.2011.09.022 PubMed DOI PMC
Roca-Cusachs P., Conte V., Trepat X. (2017). Quantifying forces in cell biology. Nat. Cell Biol. 19 742–751. 10.1038/ncb3564 PubMed DOI
Rocha M. S. (2015). Extracting physical chemistry from mechanics: a new approach to investigate DNA interactions with drugs and proteins in single molecule experiments. Integr. Biol. 7 967–986. 10.1039/C5IB00127G PubMed DOI
Rosenbluth M. J., Lam W. A., Fletcher D. A. (2006). Force microscopy of nonadherent cells: a comparison of leukemia cell deformability. Biophys. J. 90 2994–3003. 10.1529/biophysj.105.067496 PubMed DOI PMC
Roth K. B., Eggleton C. D., Neeves K. B., Marr D. W. M. (2013). Measuring cell mechanics by optical alignment compression cytometry. Lab Chip 13 1571–1577. 10.1039/c3lc41253a PubMed DOI PMC
Saphirstein R. J., Gao Y. Z., Jensen M. H., Gallant C. M., Vetterkind S., Moore J. R., et al. (2013). The focal adhesion: a regulated component of aortic stiffness. PLoS One 8:e62461. 10.1371/journal.pone.0062461 PubMed DOI PMC
Sato H., Kataoka N., Kajiya F., Katano M., Takigawa T., Masuda T. (2004). Kinetic study on the elastic change of vascular endothelial cells on collagen matrices by atomic force microscopy. Colloids Surf. B Biointerfaces 34 141–146. 10.1016/j.colsurfb.2003.12.013 PubMed DOI
Scuor N., Gallina P., Panchawagh H. V., Mahajan R. L., Sbaizero O., Sergo V. (2006). Design of a novel MEMS platform for the biaxial stimulation of living cells. Biomed. Microdevices 8 239–246. 10.1007/s10544-006-8268-3 PubMed DOI
Serrao G. W., Turnbull I. C., Ancukiewicz D., Kim D. E., Kao E., Cashman T. J., et al. (2012). Myocyte-depleted engineered cardiac tissues support therapeutic potential of mesenchymal stem cells. Tissue Eng. Part A 18 1322–1333. 10.1089/ten.TEA.2011.0278 PubMed DOI PMC
Shang H., Lee G. U. (2007). Magnetic tweezers measurement of the bond lifetime-force behavior of the IgG-protein a specific molecular interaction. J. Am. Chem. Soc. 129 6640–6646. 10.1021/JA071215C PubMed DOI
Shao Y., Fu J. (2014). Integrated micro/nanoengineered functional biomaterials for cell mechanics and mechanobiology: a materials perspective. Adv. Mater. 26 1494–1533. 10.1002/adma.201304431 PubMed DOI PMC
Shiu J. Y., Aires L., Lin Z., Vogel V. (2018). Nanopillar force measurements reveal actin-cap-mediated YAP mechanotransduction. Nat. Cell Biol. 20 262–271. 10.1038/s41556-017-0030-y PubMed DOI
Shiu Y.-T., Li S., Marganski W. A., Usami S., Schwartz M. A., Wang Y.-L., et al. (2004). Rho mediates the shear-enhancement of endothelial cell migration and traction force generation. Biophys. J. 86 2558–2565. 10.1016/S0006-3495(04)74311-8 PubMed DOI PMC
Shroff S. G., Saner D. R., Lal R. (1995). Dynamic micromechanical properties of cultured rat atrial myocytes measured by atomic force microscopy. Am. J. Physiol. Physiol. 269 C286–C292. 10.1152/ajpcell.1995.269.1.C286 PubMed DOI
Silberberg Y. R., Pelling A. E., Yakubov G. E., Crum W. R., Hawkes D. J., Horton M. A. (2008). Mitochondrial displacements in response to nanomechanical forces. J. Mol. Recognit. 21 30–36. 10.1002/jmr.868 PubMed DOI
Sims P. A., Xie X. S. (2009). Probing dynein and kinesin stepping with mechanical manipulation in a living cell. Chemphyschem 10 1511–1516. 10.1002/cphc.200900113 PubMed DOI PMC
Sneddon I. N. (1965). The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int. J. Eng. Sci. 3 47–57. 10.1016/0020-7225(65)90019-4 PubMed DOI
Sniadecki N. J., Anguelouch A., Yang M. T., Lamb C. M., Liu Z., Kirschner S. B., et al. (2007). Magnetic microposts as an approach to apply forces to living cells. Proc. Natl. Acad. Sci. U.S.A. 104 14553–14558. 10.1073/pnas.0611613104 PubMed DOI PMC
Sparkes I., White R. R., Coles B., Botchway S. W., Ward A. (2018). “Using optical tweezers combined with total internal reflection microscopy to study interactions between the ER and Golgi in plant cells,” in The Plant Endoplasmic Reticulum : Methods and Protocols, eds Hawes C., Kriechbaumer V. (New York, NY: Springer; ), 167–178. 10.1007/978-1-4939-7389-7_13 PubMed DOI
Staunton J. R., Blehm B., Devine A., Tanner K. (2017). In situ calibration of position detection in an optical trap for active microrheology in viscous materials. Opt. Express 25 1746–1761. 10.1364/OE.25.001746 PubMed DOI PMC
Steinwachs J., Metzner C., Skodzek K., Lang N., Thievessen I., Mark C., et al. (2016). Three-dimensional force microscopy of cells in biopolymer networks. Nat. Methods 13 171–176. 10.1038/nmeth.3685 PubMed DOI
Sun N., Yazawa M., Liu J., Han L., Sanchez-Freire V., Abilez O. J., et al. (2012). Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy. Sci. Transl. Med 4:130ra47. 10.1126/scitranslmed.3003552 PubMed DOI PMC
Sun Y., Nelson B. J. (2007). MEMS capacitive force sensors for cellular and flight biomechanics. Biomed. Mater. 2 S16–S22. 10.1088/1748-6041/2/1/S03 PubMed DOI
Sun Y., Villa-Diaz L. G., Lam R. H. W., Chen W., Krebsbach P. H., Fu J. (2012). Mechanics regulates fate decisions of human embryonic stem cells. PLoS One 7:e37178. 10.1371/journal.pone.0037178 PubMed DOI PMC
Sunyer R., Conte V., Escribano J., Elosegui-Artola A., Labernadie A., Valon L., et al. (2016). Collective cell durotaxis emerges from long-range intercellular force transmission. Science 353 1157–1161. 10.1126/science.aaf7119 PubMed DOI
Suresh S., Spatz J., Mills J. P., Micoulet A., Dao M., Lim C. T., et al. (2005). Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomater. 1 15–30. 10.1016/j.actbio.2004.09.001 PubMed DOI
Szymonski M., Targosz-Korecka M., Malek-Zietek K. E. (2015). Nano-mechanical model of endothelial dysfunction for AFM-based diagnostics at the cellular level. Pharmacol. Rep. 67 728–735. 10.1016/J.PHAREP.2015.05.003 PubMed DOI
Tabdili H., Langer M., Shi Q., Poh Y.-C., Wang N., Leckband D. (2012). Cadherin-dependent mechanotransduction depends on ligand identity but not affinity. J. Cell Sci. 125 4362–4371. 10.1242/jcs.105775 PubMed DOI PMC
Takahashi H., Jung U. G., Kan T., Tsukagoshi T., Matsumoto K., Shimoyama I. (2016). Rigid two-axis MEMS force plate for measuring cellular traction force. J. Micromech. Microeng. 26:105006 10.1088/0960-1317/26/10/105006 DOI
Tan J. L., Tien J., Pirone D. M., Gray D. S., Bhadriraju K., Chen C. S. (2003). Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad. Sci. U.S.A. 100 1484–1489. 10.1073/pnas.0235407100 PubMed DOI PMC
Tanase M., Biais N., Sheetz M. (2007). Magnetic tweezers in cell biology. Methods Cell Biol. 83 473–493. 10.1016/S0091-679X(07)83020-2 PubMed DOI
Tatara Y. (1989). Extensive theory of force-approach relations of elastic spheres in compression and in impact. J. Eng. Mater. Technol. 111:163 10.1115/1.3226449 DOI
Tavacoli J. W., Bauër P., Fermigier M., Bartolo D., Heuvingh J., du Roure O. (2013). The fabrication and directed self-assembly of micron-sized superparamagnetic non-spherical particles. Soft Matter 9:9103 10.1039/c3sm51589c DOI
Thoumine O., Kocian P., Kottelat A., Meister J. J. (2000). Short-term binding of fibroblasts to fibronectin: optical tweezers experiments and probabilistic analysis. Eur. Biophys. J. 29 398–408. 10.1007/s002490000087 PubMed DOI
Titushkin I., Cho M. (2006). Distinct membrane mechanical properties of human mesenchymal stem cells determined using laser optical tweezers. Biophys. J. 90 2582–2591. 10.1529/biophysj.105.073775 PubMed DOI PMC
Topal T., Hong X., Xue X., Fan Z., Kanetkar N., Nguyen J. T., et al. (2018). Acoustic tweezing cytometry induces rapid initiation of human embryonic stem cell differentiation. Sci. Rep. 8:12977. 10.1038/s41598-018-30939-z PubMed DOI PMC
Trepat X., Deng L., An S. S., Navajas D., Tschumperlin D. J., Gerthoffer W. T., et al. (2007). Universal physical responses to stretch in the living cell. Nature 447 592–595. 10.1038/nature05824 PubMed DOI PMC
Trepat X., Wasserman M. R., Angelini T. E., Millet E., Weitz D. A., Butler J. P., et al. (2009). Physical forces during collective cell migration. Nat. Phys. 5 426–430. 10.1038/nphys1269 DOI
Usukura E., Narita A., Yagi A., Ito S., Usukura J. (2016). An unroofing method to observe the cytoskeleton directly at molecular resolution using atomic force microscopy. Sci. Rep. 6:27472. 10.1038/srep27472 PubMed DOI PMC
Usukura J., Yoshimura A., Minakata S., Youn D., Ahn J., Cho S.-J. (2012). Use of the unroofing technique for atomic force microscopic imaging of the intra-cellular cytoskeleton under aqueous conditions. J. Electron Microsc. 61 321–326. 10.1093/jmicro/dfs055 PubMed DOI
Veraitch F., Hernandez D., Mason C., Pelling A. E., Veraitch F. S. (2011). Precisely delivered nanomechanical forces induce blebbing in undifferentiated mouse embryonic stem cells. Cell Health Cytoskelet. 3 23–34. 10.2147/CHC.S13863 DOI
Voiculescu I., Nordin A. N. (2012). Acoustic wave based MEMS devices for biosensing applications. Biosens. Bioelectron. 33 1–9. 10.1016/J.BIOS.2011.12.041 PubMed DOI
Wang J. H.-C., Li B. (2010). “The principles and biological applications of cell traction force microscopy,” in Microscopy : Science, Technology, Applications and Education, eds Méndez-Vilas A., Díaz J. (Badajoz: Formatex Research Center; ), 449–458.
Wang N., Butler J. P., Ingber D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260 1124–1127. 10.1126/science.7684161 PubMed DOI
Wang X., Yang Y., Hu X., Kawazoe N., Yang Y., Chen G. (2016). Morphological and mechanical properties of osteosarcoma microenvironment cells explored by atomic force microscopy. Anal. Sci. 32 1177–1182. 10.2116/analsci.32.1177 PubMed DOI
Wang Y., Botvinick E. L., Zhao Y., Berns M. W., Usami S., Tsien R. Y., et al. (2005). Visualizing the mechanical activation of Src. Nature 434 1040–1045. 10.1038/nature03469 PubMed DOI
Wei M.-T., Zaorski A., Yalcin H. C., Wang J., Hallow M., Ghadiali S. N., et al. (2008). A comparative study of living cell micromechanical properties by oscillatory optical tweezers. Opt. Express 16 8594–8603. 10.1364/OE.16.008594 PubMed DOI
Wu J., Du G. (1990). Acoustic radiation force on a small compressible sphere in a focused beam. J. Acoust. Soc. Am. 87 997–1003. 10.1121/1.399435 DOI
Wu J. R. (1991). Acoustical tweezers. J. Acoust. Soc. Am. 89 2140–2143. 10.1121/1.400907 PubMed DOI
Xiang Y., LaVan D. A. (2007). Analysis of soft cantilevers as force transducers. Appl. Phys. Lett. 90:133901. 10.1063/1.2716376 PubMed DOI
Xin Q., Li P., He Y., Shi C., Qiao Y., Bian X., et al. (2017). Magnetic tweezers for the mechanical research of DNA at the single molecule level. Anal. Methods 9 5720–5730. 10.1039/C7AY01495C DOI
Xue X., Hong X., Li Z., Deng C. X., Fu J. (2017). Acoustic tweezing cytometry enhances osteogenesis of human mesenchymal stem cells through cytoskeletal contractility and YAP activation. Biomaterials 134 22–30. 10.1016/j.biomaterials.2017.04.039 PubMed DOI PMC
Yalcin H. C., Hallow K. M., Wang J., Wei M. T., Ou-Yang H. D., Ghadiali S. N. (2009). Influence of cytoskeletal structure and mechanics on epithelial cell injury during cyclic airway reopening. Am. J. Physiol. Lung Cell. Mol. Physiol. 297 L881–L891. 10.1152/ajplung.90562.2008 PubMed DOI
Yan B., Ren J., Liu Y., Huang H., Zheng X., Zou Q. (2017). Study of cholesterol repletion effect on nanomechanical properties of human umbilical vein endothelial cell via rapid broadband atomic force microscopy. J. Biomech. Eng. 139:034501. 10.1115/1.4035260 PubMed DOI
Yang M. T., Fu J., Wang Y.-K., Desai R. A., Chen C. S. (2011). Assaying stem cell mechanobiology on microfabricated elastomeric substrates with geometrically modulated rigidity. Nat. Protoc. 6 187–213. 10.1038/nprot.2010.189 PubMed DOI PMC
Yang S., Saif T. (2005). Micromachined force sensors for the study of cell mechanics. Rev. Sci. Instrum. 76:044301 10.1063/1.1863792 DOI
Yang M. T., Sniadecki N. J., Chen C. S. (2007). Geometric considerations of micro- to nanoscale elastomeric post arrays to study cellular traction forces. Adv. Mater. 19 3119–3123. 10.1002/adma.200701956 DOI
Yang Z., Lin J.-S., Chen J., Wang J. H.-C. (2006). Determining substrate displacement and cell traction fields—a new approach. J. Theor. Biol. 242 607–616. 10.1016/J.JTBI.2006.05.005 PubMed DOI
Zemła J., Danilkiewicz J., Orzechowska B., Pabijan J., Seweryn S., Lekka M. (2018). Atomic force microscopy as a tool for assessing the cellular elasticity and adhesiveness to identify cancer cells and tissues. Semin. Cell Dev. Biol. 73 115–124. 10.1016/j.semcdb.2017.06.029 PubMed DOI
Zhang H., Liu K.-K. (2008). Optical tweezers for single cells. J. R. Soc. Interface 5 671–690. 10.1098/rsif.2008.0052 PubMed DOI PMC
Zhang J. S., Kraus W. E., Truskey G. A. (2004). Stretch-induced nitric oxide modulates mechanical properties of skeletal muscle cells. Am. J. Physiol. Physiol. 287 C292–C299. 10.1152/ajpcell.00018.2004 PubMed DOI
Zhang L., Dong J. (2012). Design, fabrication, and testing of a SOI-MEMS-based active microprobe for potential cellular force sensing applications. Adv. Mech. Eng. 4: 785798 10.1155/2012/785798 DOI
Zhang Y., DaSilva M., Ashall B., Doyle G., Zerulla D., Sands T. D., et al. (2011). Magnetic manipulation and optical imaging of an active plasmonic single-particle Fe–Au nanorod. Langmuir 27 15292–15298. 10.1021/la203863p PubMed DOI
Zhang Y., Wang Q. (2012). Magnetic-plasmonic dual modulated FePt-Au ternary heterostructured nanorods as a promising nano-bioprobe. Adv. Mater. 24 2485–2490. 10.1002/adma.201103991 PubMed DOI
Zhao X., Zhong Y., Ye T., Wang D., Mao B. (2015). Discrimination between cervical cancer cells and normal cervical cells based on longitudinal elasticity using atomic force microscopy. Nanoscale Res. Lett. 10:482. 10.1186/s11671-015-1174-y PubMed DOI PMC
Zhao X.-H., Laschinger C., Arora P., Szaszi K., Kapus A., McCulloch C. A. (2007). Force activates smooth muscle actin promoter activity through the Rho signaling pathway. J. Cell Sci. 120 1801–1809. 10.1242/jcs.001586 PubMed DOI
Zhao Y., Lim C. C., Sawyer D. B., Liao R., Zhang X. (2005). Cellular force measurements using single-spaced polymeric microstructures: isolating cells from base substrate. J. Micromech. Microeng. 15 1649–1656. 10.1088/0960-1317/15/9/006 DOI
Zheng X. R., Zhang X. (2011). Microsystems for cellular force measurement: a review. J. Micromech. Microeng. 21:054003. 10.1088/0960-1317/21/5/054003 PubMed DOI
Zhong M.-C., Wei X.-B., Zhou J.-H., Wang Z.-Q., Li Y.-M. (2013). Trapping red blood cells in living animals using optical tweezers. Nat. Commun. 4:1768. 10.1038/ncomms2786 PubMed DOI
Ziemann F., Rädler J., Sackmann E. (1994). Local measurements of viscoelastic moduli of entangled actin networks using an oscillating magnetic bead micro-rheometer. Biophys. J. 66 2210–2216. 10.1016/S0006-3495(94)81017-3 PubMed DOI PMC
A primer to traction force microscopy