Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-04T21:17:05.717Z Has data issue: false hasContentIssue false
  • English
  • Français

Atomic Force Microscopy for Tumor Research at Cell and Molecule Levels

Published online by Cambridge University Press:  08 March 2022

Yitong Qin ,
Wenguang Yang Open the ORCID record for Wenguang Yang [Opens in a new window] ,
Honghui Chu ,
Yan Li ,
Shuxiang Cai ,
Haibo Yu  and
Lianqing Liu
Yitong Qin
Affiliation:
School of Electromechanical and Automotive Engineering, Yantai University, Yantai 264005, China
Wenguang Yang*
Affiliation:
School of Electromechanical and Automotive Engineering, Yantai University, Yantai 264005, China
Honghui Chu
Affiliation:
School of Electromechanical and Automotive Engineering, Yantai University, Yantai 264005, China
Yan Li
Affiliation:
School of Electromechanical and Automotive Engineering, Yantai University, Yantai 264005, China
Shuxiang Cai
Affiliation:
School of Electromechanical and Automotive Engineering, Yantai University, Yantai 264005, China
Haibo Yu
Affiliation:
State Key Laboratory of Robotics, Shenyang Institute of Automation, Chinese Academy of Sciences, Shenyang 110016, China
Lianqing Liu
Affiliation:
State Key Laboratory of Robotics, Shenyang Institute of Automation, Chinese Academy of Sciences, Shenyang 110016, China
*
*Corresponding author: Wenguang Yang, E-mail: [email protected]
Get access

Abstract

Tumors have posed a serious threat to human life and health. Researchers can determine whether or not cells are cancerous, whether the cancer cells are invasive or metastatic, and what the effects of drugs are on cancer cells by the physical properties such as hardness, adhesion, and Young's modulus. The atomic force microscope (AFM) has emerged as a key important tool for biomechanics research on tumor cells due to its ability to image and collect force spectroscopy information of biological samples with nano-level spatial resolution and under near-physiological conditions. This article reviews the existing results of the study of cancer cells with AFM. The main foci are the operating principle of AFM and research advances in mechanical property measurement, ultra-microtopography, and molecular recognition of tumor cells, which allows us to outline what we do know it in a systematic way and to summarize and to discuss future directions.

Keywords

atomic force microscopemechanical characteristicsmolecular recognitionultramicrotopography
Type
Review Article
Information
Microscopy and Microanalysis , Volume 28 , Issue 3 , June 2022 , pp. 585 - 602
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abidine, Y, Constantinescu, A, Laurent, VM, Rajan, VS, Michel, R, Laplaud, V, Duperray, A & Verdier, C (2018). Mechanosensitivity of cancer cells in contact with soft substrates using AFM. Biophys J 114, 1165.CrossRefGoogle ScholarPubMed
Almonte, L & Colchero, J (2017). True non-contact atomic force microscopy imaging of heterogeneous biological samples in liquids: Topography and material contrast. Nanoscale 9, 2903–2915.CrossRefGoogle ScholarPubMed
Baker, M (2010). Making membrane proteins for structures: A trillion tiny tweaks. Nat Methods 7, 429–434.CrossRefGoogle ScholarPubMed
Binnig, G, Quate, CF & Gerber, CH (1986). Atomic force microscope. Phys Rev Lett 56, 930–933.CrossRefGoogle ScholarPubMed
Bonfiglio, A, Parodi, MT & Tonini, GP (1995). Subcellular details of early events of differentiation induced by retinoic acid in human neuroblastoma cells detected by atomic force microscope. Exp Cell Res 216, 73–79.CrossRefGoogle ScholarPubMed
Brown, KA, Berezovsky, J & Westervelt, RM (2011). Coaxial atomic force microscope probes for imaging with dielectrophoresis. Appl Phys Lett 98, 183103.CrossRefGoogle ScholarPubMed
Cias, G, Sassun, TE, Minelli, E, Antonelli, M & Spirito, M (2016). Nano-mechanical signature of brain tumours. Nanoscale 8, 19629–19643.Google Scholar
Collett, S, Torresi, J, Earnest-Silveira, L, Christiansen, D, Elbourne, A & Ramsland, PA (2019). Probing and pressing surfaces of hepatitis C virus-like particles. J Colloid Interface Sci 545, 259–268.CrossRefGoogle ScholarPubMed
Cricenti, A, Generosi, R, Girasole, M, Scarselli, MA, Perfetti, P, Bach, S & Colizzi, V (1999). Atomic force microscopy observation of human lymphoid cells chronically infected with the human immunodeficiency virus. J Vac Sci Technol A 17, 1141–1144.CrossRefGoogle Scholar
Cross, SE, Jin, Y-S, Rao, J & Gimzewski, JK (2007). Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol 2, 780–783.CrossRefGoogle ScholarPubMed
Dague, E, Alsteens, D, Latgé, J-P & Dufrêne, YF (2008). High-resolution cell surface dynamics of germinating Aspergillus fumigatus conidia. Biophys J 94, 656–660.CrossRefGoogle ScholarPubMed
Derjaguin, BV, Muller, VM & Toporov, YP (1975). Effect of contact deformations on the adhesion of particles. J Colloid Interface Sci 53, 314–326.CrossRefGoogle Scholar
Dimitriadis, EK, Horkay, F, Maresca, J, Kachar, B & Chadwick, RS (2002). Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys J 82, 2798–2810.CrossRefGoogle ScholarPubMed
Dufrêne, YF, Ando, T, Garcia, R, Alsteens, D, Martinez-Martin, D, Engel, A, Gerber, C & Müller, DJJNN (2017). Imaging modes of atomic force microscopy for application in molecular and cell biology. Nat Nanotechnol 12, 295–307.CrossRefGoogle ScholarPubMed
Dufrêne, YF & Yves, F (2008). Towards nanomicrobiology using atomic force microscopy. Nat Rev Microbiol 6, 674–680.CrossRefGoogle ScholarPubMed
Dupres, V, Alsteens, D, Andre, G, Verbelen, C & Dufrêne, YF (2009). Fishing single molecules on live cells. Nano Today 4, 262–268.CrossRefGoogle Scholar
Feng, RM, Zong, YN, Cao, SM & Xu, RH (2019). Current cancer situation in China: Good or bad news from the 2018 global cancer statistics? Cancer Commun (Lond) 39, 22.CrossRefGoogle ScholarPubMed
Ferlay, J, Colombet, M, Soerjomataram, I, Mathers, C, Parkin, DM, Pineros, M, Znaor, A & Bray, F (2019). Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer 144, 1941–1953.CrossRefGoogle ScholarPubMed
Fletcher, DA & Mullins, RD (2010). Cell mechanics and the cytoskeleton. Nature 463, 485–492.CrossRefGoogle ScholarPubMed
Fotiadis, D (2012). Atomic force microscopy for the study of membrane proteins. Curr Opin Biotechnol 23, 510–515.CrossRefGoogle Scholar
Friedrichs, J, Legate, KR, Schubert, R, Bharadwaj, M & Benoit, M (2013). A practical guide to quantify cell adhesion using single-cell force spectroscopy. Methods 60, 169–178.CrossRefGoogle ScholarPubMed
Gan, C, Ao, M, Liu, Z & Chen, Y (2015). Imaging and force measurement of LDL and HDL by AFM in air and liquid. FEBS Open Bio 5, 276–282.CrossRefGoogle Scholar
Garcia, PD, Guerrero, CR & Garcia, R (2020). Nanorheology of living cells measured by AFM-based force–distance curves. Nanoscale 12, 9133–9143.CrossRefGoogle ScholarPubMed
Garcia, R (2020). Nanomechanical mapping of soft materials with the atomic force microscope: Methods, theory and applications. Eng Technol 49, 5850–5884.Google Scholar
Gómez-Varela, AI, Stamov, DR, Miranda, A, Alves, R, Barata-Antunes, C, Dambournet, D, Drubin, DG, Paiva, S & De Beule, PAA (2020). Simultaneous co-localized super-resolution fluorescence microscopy and atomic force microscopy: Combined SIM and AFM platform for the life sciences. Sci Rep 10, 1122.CrossRefGoogle ScholarPubMed
Graham, HK, Hodson, NW, Hoyland, JA, Millward-Sadler, SJ, Garrod, D, Scothern, A, Griffiths, CEM, Watson, REB, Cox, TR, Erler, JT, Trafford, AW & Sherratt, MJ (2010). Tissue section AFM: In situ ultrastructural imaging of native biomolecules. Matrix Biol 29, 254–260.CrossRefGoogle ScholarPubMed
Greenleaf, WJ, Woodside, MT & Block, SM (2007). High-resolution single-molecule measurements of biomolecular motion. Annu Rev Biophys Biomol Struct 36, 171.CrossRefGoogle ScholarPubMed
Gross, L, Mohn, F, Moll, N, Liljeroth, P & Meyer, G (2009). The chemical structure of a molecule resolved by atomic force microscopy. Science 325, 1110–1114.CrossRefGoogle ScholarPubMed
Guo, S, Ray, C, Kirkpatrick, A, Lad, N & Akhremitchev, BB (2008). Effects of multiple-bond ruptures on kinetic parameters extracted from force spectroscopy measurements: Revisiting biotin-streptavidin interactions. Biophys J 95, 3964–3976.CrossRefGoogle ScholarPubMed
Hanahan, D & Weinberg, RA (2000). The hallmarks of cancer. Cell 100, 57–70.CrossRefGoogle ScholarPubMed
Heuberger, M (1996). Elastic deformations of tip and sample during atomic force microscope measurements. J Vac Sci Technol B Microelectron Nanometer Struct 14, 1250–1254.CrossRefGoogle Scholar
Hinck, L & Näthke, I (2014). Changes in cell and tissue organization in cancer of the breast and colon. Curr Opin Cell Biol 26, 87–95.CrossRefGoogle ScholarPubMed
Hu, M, Wang, J, Zhao, H, Dong, S & Cai, J (2009). Nanostructure and nanomechanics analysis of lymphocyte using AFM: From resting, activated to apoptosis. J Biomech 42, 1513–1519.CrossRefGoogle Scholar
Huml, M, Silye, R, Zauner, G, Hutterer, S & Schilcher, K (2013). Brain tumor classification using AFM in combination with data mining techniques. BioMed Res Int 2013, 176519.CrossRefGoogle ScholarPubMed
Johnson, KL, Kendall, K & Roberts, A (1971). Surface energy and the contact of elastic solids. Proc R Soc Lond A Math Phys Sci 324, 301–313.Google Scholar
Johnson, WT, Kada, G, Stroh, C, Gruber, H, Wang, H, Kienberger, F, Ebner, A, Lindsay, S & Hinterdorfer, P (2005). Simultaneous topography and RECognition mapping with PicoTREC™: A powerful new technology that can be used to map nanometer-scale molecular binding sites on a variety of surfaces. pp. 679–682.Google Scholar
Kada, G, Kienberger, F & Hinterdorfer, P (2008). Atomic force microscopy in bionanotechnology. Nano Today 3, 12–19.CrossRefGoogle Scholar
Kasas, S, Longo, G & Dietler, G (2013). Mechanical properties of biological specimens explored by atomic force microscopy. J Phys D Appl Phys 46, 133001.CrossRefGoogle Scholar
Kaul-Ghanekar, R, Singh, S, Mamgain, H, Jalota-Badhwar, A, Paknikar, KM & Chattopadhyay, S (2009). Tumor suppressor protein SMAR1 modulates the roughness of cell surface: Combined AFM and SEM study. BMC Cancer 9, 1–12.CrossRefGoogle ScholarPubMed
Kim, H, Yamagishi, A, Imaizumi, M, Onomura, Y, Nagasaki, A, Miyagi, Y, Okada, T & Nakamura, C (2017). Quantitative measurements of intercellular adhesion between a macrophage and cancer cells using a cup-attached AFM chip. Colloids & Surf B Biointerfaces 155, 366.CrossRefGoogle ScholarPubMed
Kondra, S, Laishram, J, Ban, J, Migliorini, E, Foggia, VD, Lazzarino, M, Torre, V & Ruaro, ME (2009). Integration of confocal and atomic force microscopy images. J Neurosci Methods 177, 94–107.CrossRefGoogle ScholarPubMed
Kuznetsova, TG, Starodubtseva, MN, Yegorenkov, NI, Chizhik, SA & Zhdanov, RI (2007). Atomic force microscopy probing of cell elasticity. Micron 38, 824–833.CrossRefGoogle ScholarPubMed
Lekka, M (2016). Discrimination between normal and cancerous cells using AFM. BioNanoScience 6, 65–80.CrossRefGoogle ScholarPubMed
Lekka, M, Laidler, P, Gil, D, Lekki, J, Stachura, Z & Hrynkiewicz, AZ (1999). Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Eur Biophys J 28, 312–316.CrossRefGoogle ScholarPubMed
Li, M, Liu, L-Q, Xi, N & Wang, Y-C (2015 a). Nanoscale monitoring of drug actions on cell membrane using atomic force microscopy. Acta Pharmacol Sin 36, 769–782.CrossRefGoogle ScholarPubMed
Li, M, Liu, L-Q, Xi, N, Wang, Y-C, Dong, Z-L, Xiao, X-B & Zhang, W-J (2012). Drug-induced changes of topography and elasticity in living B lymphoma cells based on atomic force microscopy. Acta Phys Chim Sin 28, 1502–1508.Google Scholar
Li, M, Liu, L-Q, Xi, N, Wang, Y-C & Wang, W (2015 b). Imaging and mapping individual target proteins on clinical lymphoma cells by AFM. 9th IEEE International Conference on Nano/Molecular Medicine & Engineering (NANOMED), pp. 84–87. IEEE.CrossRefGoogle Scholar
Li, P, Zhou, J, Li, W, Wu, H & Long, M (2020). Characterizing liver sinusoidal endothelial cell fenestrae on soft substrates upon AFM imaging and deep learning. Biochim Biophys Acta (BBA) - Gen Subj 1864, 129702.CrossRefGoogle ScholarPubMed
Li, QS, Lee, GYH, Ong, CN & Lim, CT (2008). AFM indentation study of breast cancer cells. Biochem Biophys Res Commun 374, 609–613.CrossRefGoogle ScholarPubMed
Liu, F & Tschumperlin, DJ (2011). Micro-mechanical characterization of lung tissue using atomic force microscopy. J Vis Exp Jove 54, e2911.Google Scholar
Liu, S & Wang, Y (2010). Application of AFM in microbiology: A review. Scanning 32, 61.CrossRefGoogle ScholarPubMed
Liu, X, Feng, X, Williams, RO & Zhang, F (2018). Characterization of amorphous solid dispersions. J Pharm Invest 48, 19–41.CrossRefGoogle Scholar
Ma, X, Qu, X, Zhu, W, Li, Y-S, Yuan, S, Zhang, H, Liu, J, Wang, P, Lai, CSE, Zanella, F, Feng, G-S, Sheikh, F, Chien, S & Chen, S (2016). Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc Natl Acad Sci USA 113, 2206–2211.CrossRefGoogle ScholarPubMed
Mikihiro, S, Hiroki, W, Takayuki, U, Toshio, A & Ryohei, Y (2017). High-speed atomic force microscopy imaging of live mammalian cells. Biophys Physicobiol 14, 127–135.Google Scholar
Milburn, C, Zhou, J, Bravo, O, Kumar, C & Soboyejo, WO (2005). Sensing interactions between vimentin antibodies and antigens for early cancer detection. J Biomed Nanotechnol 1, 30–38.CrossRefGoogle Scholar
Moreno-Cencerrado, A, Iturri, J, Pecorari, I, Dm Vivanco, M, Sbaizero, O & Toca-Herrera, JL (2017). Investigating cell-substrate and cell–cell interactions by means of single-cell-probe force spectroscopy. Microsc Res Tech 80, 124–130.CrossRefGoogle ScholarPubMed
Müller, DJ & Engel, A (2007). Atomic force microscopy and spectroscopy of native membrane proteins. Nat Protoc 2, 2191–2197.CrossRefGoogle ScholarPubMed
Müller, DJ, Schabert, FA, Büldt, G & Engel, A (1995). Imaging purple membranes in aqueous solutions at sub-nanometer resolution by atomic force microscopy. Biophys J 68, 1681–1686.CrossRefGoogle ScholarPubMed
Nishita, K & Manonmani, H (2015) Changes in cell membrane morphology of colon cancer cells (HCT116) after treatment with azurin derived hexapeptide 4 by AFM and STEM. Int J Innov Res Sci Eng Technol, 4, 11550–11557.Google Scholar
O'donoghue, MB, Shi, X, Fang, X & Tan, W (2012). Single-molecule atomic force microscopy on live cells compares aptamer and antibody rupture forces. Anal Bioanal Chem 402, 3205–3209.CrossRefGoogle ScholarPubMed
Omidvar, R, Tafazzoli-Shadpour, M, Shokrgozar, MA & Rostami, M (2014). Atomic force microscope-based single cell force spectroscopy of breast cancer cell lines: An approach for evaluating cellular invasion. J Biomech 47, 3373–3379.CrossRefGoogle ScholarPubMed
Perez-Guaita, D, Kochan, K, Batty, M, Doerig, C, Garcia-Bustos, J, Espinoza, S, Mcnaughton, D, Heraud, P & Wood, BR (2018). Multispectral atomic force microscopy-infrared nano-imaging of malaria infected red blood cells. Anal Chem 90, 3140–3148.CrossRefGoogle ScholarPubMed
Pi, J, Jin, H, Jiang, J, Yang, F, Cai, H, Yang, P, Cai, J & Chen, ZW (2017). Single molecule force spectroscopy for in-situ probing oridonin inhibited ROS-mediated EGF-EGFR interactions in living KYSE-150 cells. Pharmacol Res 119, 479–489.CrossRefGoogle ScholarPubMed
Plodinec, M, Loparic, M & Aebi, U (2010). Imaging articular cartilage tissue using atomic force microscopy (AFM). Cold Spring Harb Protoc 2010, pdb-prot5499.CrossRefGoogle Scholar
Polacheck, WJ & Chen, CS (2016). Measuring cell-generated forces: A guide to the available tools. Nat Methods 13, 415–423.CrossRefGoogle Scholar
Puntheeranurak, T, Wildling, L, Gruber, HJ, Kinne, RKH & Hinterdorfer, P (2006). Ligands on the string: Single-molecule AFM studies on the interaction of antibodies and substrates with the Na+-glucose co-transporter SGLT1 in living cells. J Cell Sci 119, 2960–2967.CrossRefGoogle ScholarPubMed
Qin, J, Zhang, M, Guan, Y, Li, C, Ma, X, Rankl, C & Tang, J (2020). Investigation of the interaction between MeCP2 methyl-CpG binding domain and methylated DNA by single molecule force spectroscopy. Anal Chim Acta 1124, 52–59.CrossRefGoogle ScholarPubMed
Raab, A, Han, W, Badt, D, Smith-Gill, SJ, Lindsay, SM, Schindler, H & Hinterdorfer, P (1999). Antibody recognition imaging by force microscopy. Nat Biotechnol 17, 901–905.CrossRefGoogle ScholarPubMed
Raczkowska, J & Prauzner-Bechcicki, S (2016). Precise positioning of cancerous cells on PDMS substrates with gradients of elasticity. Biomed Microdevices 18, 90.CrossRefGoogle ScholarPubMed
Roca-Cusachs, P, Conte, V & Trepat, X (2017). Quantifying forces in cell biology. Nat Cell Biol 19, 742–751.CrossRefGoogle ScholarPubMed
Rother, J, Noding, H, Mey, I & Janshoff, A (2014). Atomic force microscopy-based microrheology reveals significant differences in the viscoelastic response between malign and benign cell lines. Open Biology 4, 140046.CrossRefGoogle ScholarPubMed
Rotsch, C, Jacobson, K, Condeelis, J & Radmacher, M (2001). EGF-stimulated lamellipod extension in adenocarcinoma cells. Ultramicroscopy 86, 97–106.CrossRefGoogle ScholarPubMed
Rotsch, C & Radmacher, M (2000). Drug-Induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophys J 78, 520–535.CrossRefGoogle Scholar
Seo, YH, Jo, YN, Oh, YJ & Park, S (2015). Nano-mechanical reinforcement in drug-resistant ovarian cancer cells. Biol Pharm Bull 38, 389–395.CrossRefGoogle ScholarPubMed
Smolyakov, G, Thiebot, B, Campillo, C, Labdi, S, Severac, C, Pelta, J & Dague, É (2016). Elasticity, adhesion, and tether extrusion on breast cancer cells provide a signature of their invasive potential. ACS Appl Mater Interfaces 8, 27426–27431.CrossRefGoogle ScholarPubMed
Sneddon, IN (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.CrossRefGoogle Scholar
Staunton, JR, Doss, BL, Lindsay, S & Ros, R (2016). Correlating confocal microscopy and atomic force indentation reveals metastatic cancer cells stiffen during invasion into collagen I matrices. Sci Rep 6, 1–15.CrossRefGoogle ScholarPubMed
Stroh, CM, Ebner, A, Geretschl?Ger, M, Freudenthaler, G, Kienberger, F, Kamruzzahan, ASM, Smith-Gill, SJ, Gruber, HJ & Hinterdorfer, P (2004). Simultaneous topography and recognition imaging using force microscopy. Biophys J 87, 1981–1990.CrossRefGoogle ScholarPubMed
Suresh, S (2007). Nanomedicine: Elastic clues in cancer detection. Nat Nanotechnol 2, 748–749.CrossRefGoogle ScholarPubMed
Szydlak, R, Majka, M, Lekka, M, Kot, M & Laidler, P (2019). AFM-based analysis of Wharton's jelly mesenchymal stem cells. Int J Mol Sci 20, 4351.CrossRefGoogle ScholarPubMed
Taubenberger, AV, Girardo, S, Träber, N, Fischer-Friedrich, E, Kräter, M, Wagner, K, Kurth, T, Richter, I, Haller, B, Binner, M, Hahn, D, Freudenberg, U, Werner, C & Guck, J (2019). 3D microenvironment stiffness regulates tumor spheroid growth and mechanics via p21 and ROCK. Adv Biosys 3, 1900128.CrossRefGoogle ScholarPubMed
Tian, M, Li, Y, Liu, W, Jin, L & Shi, Y (2015). The nanomechanical signature of liver cancer tissues and Its molecular origin. Nanoscale 7, 12998–13010.CrossRefGoogle ScholarPubMed
Toca-Herrera, JL (2019). Atomic force microscopy meets biophysics, bioengineering, chemistry, and materials science. ChemSusChem 12, 603–611.CrossRefGoogle ScholarPubMed
Verbelen, C & Dufrêne, YF (2009). Direct measurement of Mycobacterium-fibronectin interactions. Integr Biol 1, 296.CrossRefGoogle ScholarPubMed
Wang, J, Wan, Z, Liu, W, Li, L, Ren, L, Wang, X, Sun, P, Ren, L, Zhao, H, Tu, Q, Zhang, Z, Song, N & Zhang, L (2009). Atomic force microscope study of tumor cell membranes following treatment with anti-cancer drugs. Biosens Bioelectron 25, 721–727.CrossRefGoogle ScholarPubMed
Wu, Y, Fang, Y, Ren, X & Lu, H (2017). A wavelet-based AFM fast imaging method with self-tuning scanning frequency. IEEE Trans Nanotechnol 16, 1088–1098.CrossRefGoogle Scholar
Xiao, L, Chen, Q, Wu, Y, Qi, X & Zhou, A (2015). Simultaneous topographic and recognition imaging of epidermal growth factor receptor (EGFR) on single human breast cancer cells. BBA - Biomembranes 1848, 1988–1995.CrossRefGoogle ScholarPubMed
Xu, W, Roman, M, Byungkyu, K, Wang, L, John, MD, Todd, S & Batra, SK (2012). Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLoS One 7, e46609.CrossRefGoogle ScholarPubMed
Yeung, T, Georges, PC, Flanagan, LA, Marg, B, Ortiz, M, Funaki, M, Zahir, N, Ming, W, Weaver, V & Janmey, PA (2005). Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60, 24.CrossRefGoogle ScholarPubMed
Yu, J, Wang, Q, Shi, X, Ma, X, Yang, H, Chen, YG & Fang, X (2007). Single-molecule force spectroscopy study of interaction between transforming growth factor β1 and Its receptor in living cells. J Phys Chem B 111, 13619.CrossRefGoogle ScholarPubMed
Zhang, C, Li, P, Liu, L, Wang, Y, Gao, Z & Li, G (2014). Development of mechanostimulated patch-clamp system for cellular physiological study. IEEE/ASME Trans Mechatron 19, 1138–1147.CrossRefGoogle Scholar
Zhao, C, Hou, X, Peng, Z, Sun, X, Li, E, Yang, H, Lu, Y & Zhu, L (2020). Estrogen receptor alpha depletion affects the biomechanical properties and cytoskeleton rearrangements in breast cancer cells. Biochem Biophys Res Commun 525, 169–176.CrossRefGoogle Scholar