Advertisement

Nano Research

, Volume 12, Issue 4, pp 703–718 | Cite as

Advances in atomic force microscopy for single-cell analysis

  • Mi LiEmail author
  • Ning Xi
  • Yuechao Wang
  • Lianqing LiuEmail author
Review Article

Abstract

Single-cell analysis has been considered as a promising way to uncover the underlying mechanisms guiding the mysteries of life activities, which considerably complements traditional ensemble assays and yields novel insights into cell biology. The advent of atomic force microscopy (AFM) provides a potent tool for investigating the structures and properties of native biological samples at the micro/nanoscale under near-physiological conditions, which promotes the studies of single-cell behaviors. In the past decades, AFM has achieved great success in single-cell observation and manipulation for biomedical applications, demonstrating the excellent capabilities of AFM in addressing biological issues at the single-cell level with unprecedented spatiotemporal resolution. In this article, we review the recent advances in single-cell analysis that has been made with the utilization of AFM, and provide perspectives for future progression.

Keywords

atomic force microscopy single-cell analysis cellular morphology cellular mechanics cellular manipulation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 61873258, 61503372, U1613220, and 61433017), the Youth Innovation Promotion Association CAS (No. 2017243), and the CAS FEA International Partnership Program for Creative Research Teams.

References

  1. [1]
    Zhuang, X. W.; Bartley, L. E.; Babcock, H. P.; Russell, R.; Ha, T.; Herschlag, D.; Chu, S. A single-molecule study of RNA catalysis and folding. Science 2000, 288, 2048–2051.Google Scholar
  2. [2]
    Xie, X. S.; Yu, J.; Yang, W. Y. Living cells as test tubes. Science 2006, 312, 228–230.Google Scholar
  3. [3]
    Altschuler, S. J.; Wu, L. F. Cellular heterogeneity: Do differences make a difference? Cell 2010, 141, 559–563.Google Scholar
  4. [4]
    Pelkmans, L. Using cell-to-cell variability—A new era in molecular biology. Science 2012, 336, 425–426.Google Scholar
  5. [5]
    Wang, D. J.; Bodovitz, S. Single cell analysis: The new frontier in “omics”. Trends Biotechnol. 2010, 28, 281–290.Google Scholar
  6. [6]
    Newman, J. R. S.; Ghaemmaghami, S.; Ihmels, J.; Breslow, D. K.; Noble, M.; DeRisi, J. L.; Weissman, J. S. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 2006, 441, 840–846.Google Scholar
  7. [7]
    Guo, G. J.; Luc, S.; Marco, E.; Lin, T. W.; Peng, C.; Kerenyi, M. A.; Beyaz, S.; Kim, W.; Xu, J.; Das, P. P. et al. Mapping cellular hierarchy by single cell analysis of the cell surface repertoire. Cell Stem Cell 2013, 13, 492–505.Google Scholar
  8. [8]
    Patel, A. P.; Tirosh, I.; Trombetta, J. J.; Shalek, A. K.; Gillespie, S. M.; Wakimoto, H.; Cahill, D. P.; Nahed, B. V.; Curry, W. T.; Martuza, R. L. et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 2014, 344, 1396–1401.Google Scholar
  9. [9]
    Hughes, A. J.; Spelke, D. P.; Xu, Z. C.; Kang, C. C.; Schaffer, D. V., Herr, A. E. Single-cell western blotting. Nat. Methods 2014, 11, 749–755.Google Scholar
  10. [10]
    Lawson, D. A.; Bhakta, N. R.; Kessenbrock, K.; Prummel, K. D.; Yu, Y.; Takai, K.; Zhou, A.; Eyob, H.; Balakrishnan, S.; Wang, C. Y. et al. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature 2015, 526, 131–135.Google Scholar
  11. [11]
    Haase, K.; Pelling, A. E. Investigating cell mechanics with atomic force microscopy. J. R. Soc. Interface 2015, 12, 20140970.Google Scholar
  12. [12]
    Reece, A.; Xia, B. Z.; Jiang, Z. L.; Noren, B.; McBride, R.; Oakey, J. Microfluidic techniques for high throughput single cell analysis. Curr. Opin. Biotechnol. 2016, 40, 90–96.Google Scholar
  13. [13]
    Diz-Muñoz, A.; Weiner, O. D.; Fletcher, D. A. In pursuit of the mechanics that shape cell surfaces. Nat. Phys. 2018, 14, 648–652.Google Scholar
  14. [14]
    Neuman, K. C.; Nagy, A. Single-molecule force spectroscopy: Optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 2008, 5, 491–505.Google Scholar
  15. [15]
    Di Carlo, D. A mechanical biomarker of cell state in medicine. J. Lab. Autom. 2012, 17, 32–42.Google Scholar
  16. [16]
    Dufrêne, Y. F.; Ando, T.; Garcia, R.; Alsteens, D.; Martinez-Martin, D.; Engel, A.; Gerber, C., Muller, D. J. Imaging modes of atomic force microscopy for application in molecular and cell biology. Nat. Nanotechnol. 2017, 12, 295–307.Google Scholar
  17. [17]
    Oesterhelt, F.; Oesterhelt, D.; Pfeiffer, M.; Engel, A.; Gaub, H. E.; Muller, D. J. Unfolding pathways of individual bacteriorhodopsins. Science 2000, 288, 143–146.Google Scholar
  18. [18]
    Ando, T.; Uchihashi, T.; Scheuring, S. Filming biomolecular processes by high-speed atomic force microscopy. Chem. Rev. 2014, 114, 3120–3188.Google Scholar
  19. [19]
    Whited, A. M.; Park, P. S. H. Atomic force microscopy: A multifaceted tool to study membrane proteins and their interactions with ligands. Biochem. Biophys. Acta 2014, 1838, 56–68.Google Scholar
  20. [20]
    Maver, U.; Velnar, T.; Gaberšcek, M.; Planinšek, O.; Finšgar, M. Recent progressive use of atomic force microscopy in biomedical applications. TrAC Trends Anal. Chem. 2016, 80, 96–111.Google Scholar
  21. [21]
    Zemla, J.; Danilkiewicz, J.; Orzechowska, B.; Pabijan, J.; Seweryn, S.; Lekka, M. Atomic force microscopy as a tool for assessing the cellular elasticity and adhesiveness to identify cancer cells and tissues. Semin. Cell Dev. Biol. 2018, 73, 115–124.Google Scholar
  22. [22]
    Radmacher, M.; Tillmann, R. W.; Fritz, M.; Gaub, H. E. From molecules to cells: Imaging soft samples with the atomic force microscope. Science 1992, 257, 1900–1905.Google Scholar
  23. [23]
    Henderson, E.; Haydon, P. G.; Sakaguchi, D. S. Actin filament dynamics in living glial cells imaged by atomic force microscopy. Science 1992, 257, 1944–1946.Google Scholar
  24. [24]
    Eghiaian, F.; Rigato, A.; Scheuring S. Structural, mechanical, and dynamical variability of the actin cortex in living cells. Biophys. J. 2015, 108, 1330–1340.Google Scholar
  25. [25]
    Schillers, H.; Medalsy, I.; Hu, S. Q.; Slade, A. L.; Shaw, J. E. Peakforce tapping resolves individual microvilli on living cells. J. Mol. Recognit. 2016, 29, 95–101.Google Scholar
  26. [26]
    Hecht, E.; Thompson, K.; Frick, M.; Wittekindt, O. H.; Dietl, P.; Mizaikoff, B.; Kranz, C. Combined atomic force microscopy-fluorescence microscopy: Analyzing exocytosis in alveolar type II cells. Anal. Chem. 2012, 84, 5716–5722.Google Scholar
  27. [27]
    Turner, R. D.; Mesnage, S.; Hobbs, J. K.; Foster, S. J. Molecular imaging of glycan chains couples cell-wall polysaccharide architecture to bacterial cell morphology. Nat. Commun. 2018, 9, 1263.Google Scholar
  28. [28]
    Li, M.; Liu, L. Q.; Xi, N.; Wang, Y. C.; Xiao, X. B.; Zhang, W. J. Quantitative analysis of drug-induced complement-mediated cytotoxic effect on single tumor cells using atomic force microscopy and fluorescence microscopy. IEEE Trans. Nanobiosci. 2015, 14, 84–94.Google Scholar
  29. [29]
    Bippes, C. A.; Muller, D. J. High-resolution atomic force microscopy and spectroscopy of native membrane proteins. Rep. Prog. Phys. 2011, 74, 086601.Google Scholar
  30. [30]
    Formosa-Dague, C.; Duval, R. E.; Dague, E. Cell biology of microbes and pharmacology of antimicrobial drugs explored by atomic force microscopy. Semin. Cell Dev. Biol. 2018, 73, 165–176.Google Scholar
  31. [31]
    Dufrêne, Y. F. Atomic force microscopy and chemical force microscopy of microbial cells. Nat. Protoc. 2008, 3, 1132–1138.Google Scholar
  32. [32]
    Dufrêne, Y. F. Atomic force microscopy in microbiology: New structural and functional insights into the microbial cell surface. mBio 2014, 5, e01363–14.Google Scholar
  33. [33]
    Formosa, C.; Pillet, F.; Schiavone, M.; Duval, R. E.; Ressier, L.; Dague, E. Generation of living cell arrays for atomic force microscopy studies. Nat. Protoc. 2015, 10, 199–204.Google Scholar
  34. [34]
    Li, M.; Liu, L. Q.; Xi, N.; Wang, Y. C.; Dong, Z. L.; Tabata, O.; Xiao, X. B.; Zhang, W. J. Imaging and measuring the rituximab-induced changes of mechanical properties in B-lymphoma cells using atomic force microscopy. Biochem. Biophys. Res. Commun. 2011, 404, 689–694.Google Scholar
  35. [35]
    Li, M.; Liu, L. Q.; Xi, N.; Wang, Y. C.; Dong, Z. L.; Xiao, X. B.; Zhang, W. J. Progress of AFM single-cell and single-molecule morphology imaging. Chin. Sci. Bull. 2013, 58, 3177–3182.Google Scholar
  36. [36]
    Li, M.; Dang, D.; Xi, N.; Wang, Y. C.; Liu, L. Q. Nanoscale imaging and force probing of biomolecular systems using atomic force microscopy: From single molecules to living cells. Nanoscale 2017, 9, 17643–17666.Google Scholar
  37. [37]
    Plomp, M.; Leighton, T. J.; Wheeler, K. E.; Hill, H. D.; Malkin, A. J. In vitro high-resolution structural dynamics of single germinating bacterial spores. Proc. Natl. Acad. Sci. USA 2007, 104, 9644–9649.Google Scholar
  38. [38]
    Fantner, G. E.; Barbero, R. J.; Gray, D. S.; Belcher, A. M. Kinetics of antimicrobial peptide activity measured on individual bacterial cells using high-speed atomic force microscopy. Nat. Nanotechnol. 2010, 5, 280–285.Google Scholar
  39. [39]
    Sutter, M.; Faulkner, M.; Aussignargues, C.; Paasch, B. C.; Barrett, S.; Kerfeld, C. A.; Liu, L. N. Visualization of bacterial microcompartment facet assembly using high-speed atomic force microscopy. Nano Lett. 2016, 16, 1590–1595.Google Scholar
  40. [40]
    Ruan, Y.; Miyagi, A.; Wang, X. Y.; Chami, M.; Boudker, O.; Scheuring, S. Direct visualization of glutamate transporter elevator mechanism by highspeed AFM. Proc. Natl. Acad. Sci. USA 2017, 114, 1584–1588.Google Scholar
  41. [41]
    El-Kirat-Chatel, S.; Dufrêne, Y. F. Nanoscale imaging of the candidamacrophage interaction using correlated fluorescence-atomic force microscopy. ACS Nano 2012, 6, 10792–10799.Google Scholar
  42. [42]
    Colom, A.; Casuso, I.; Rico, F.; Scheuring, S. A hybrid high-speed atomic force-optical microscope for visualizing single membrane proteins on eukaryotic cells. Nat. Commun. 2013, 4, 2155.Google Scholar
  43. [43]
    Watanabe, H.; Uchihashi, T.; Kobashi, T.; Shibata, M.; Nishiyama, J.; Yasuda, R.; Ando, T. Wide-area scanner for high-speed atomic force microscopy. Rev. Sci. Instrum. 2013, 84, 053702.Google Scholar
  44. [44]
    Yoshida, A.; Sakai, N.; Uekusa, Y.; Deguchi, K.; Gilmore, J. L.; Kumeta, M.; Ito, S.; Takeyasu, K. Probing in vivo dynamics of mitochondria and cortical actin networks using high-speed atomic force/fluorescence microscopy. Genes Cells 2015, 20, 85–94.Google Scholar
  45. [45]
    Kronlage, C.; Schäfer-Herte, M.; Böning, D.; Oberleithner, H.; Fels, J. Feeling for filaments: Quantification of the cortical actin web in live vascular endothelium. Biophys. J. 2015, 109, 687–698.Google Scholar
  46. [46]
    Shekhawat, G. S.; Dravid, V. P. Nanoscale imaging of buried structures via scanning near-field ultrasound holography. Science 2005, 310, 89–92.Google Scholar
  47. [47]
    Diebold, A. C. Subsurface imaging with scanning ultrasound holography. Science 2005, 310, 61–62.Google Scholar
  48. [48]
    Tetard, L.; Passian, A.; Venmar, K. T.; Lynch, R. M.; Voy, B. H.; Shekhawat, G.; Dravid, V. P.; Thundat, T. Imaging nanoparticles in cells by nanomechanical holography. Nat. Nanotechnol. 2008, 3, 501–505.Google Scholar
  49. [49]
    Garcia, R. Probe microscopy: Images from below the surface. Nat. Nanotechnol. 2010, 5, 101–102.Google Scholar
  50. [50]
    Radmacher, M. Measuring the elastic properties of living cells by the atomic force microscope. Methods Cell Biol. 2002, 68, 67–90.Google Scholar
  51. [51]
    Kasas, S.; Longo, G.; Dietler, G. Mechanical properties of biological specimens explored by atomic force microscopy. J. Phys. D Appl. Phys. 2013, 46, 133001.Google Scholar
  52. [52]
    Gavara, N. A beginner–s guide to atomic force microscopy probing for cell mechanics. Microsc. Res. Tech. 2017, 80, 75–84.Google Scholar
  53. [53]
    Li, M.; Liu, L. Q.; Xiao, X. B.; Xi, N.; Wang, Y. C. Viscoelastic properties measurement of human lymphocytes by atomic force microscopy based on magnetic beads cell isolation. IEEE Trans. Nanobiosci. 2016, 15, 398–411.Google Scholar
  54. [54]
    Lekka, M. Discrimination between normal and cancerous cells using AFM. Bionanoscience 2016, 6, 65–80.Google Scholar
  55. [55]
    Stolz, M.; Raiteri, R.; Daniels, A. U.; VanLandingham, M. R.; Baschong, W.; Aebi, U. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophys. J. 2004, 86, 3269–3283.Google Scholar
  56. [56]
    Gavara, N.; Chadwick, R. S. Determination of the elastic moduli of thin samples and adherent cells using conical atomic force microscope tips. Nat. Nanotechnol. 2012, 7, 733–736.Google Scholar
  57. [57]
    Alcaraz, J.; Buscemi, L.; Grabulosa, M.; Trepat, X.; Fabry, B.; Farré, R.; Navajas, D. Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys. J. 2003, 84, 2071–2079.Google Scholar
  58. [58]
    Rigato, A.; Miyagi, A.; Scheuring, S.; Rico, F. High-frequency microrheology reveals cytoskeleton dynamics in living cells. Nat. Phys. 2017, 13, 771–775.Google Scholar
  59. [59]
    Cross, S. E.; Jin, Y. S.; Rao, J. Y.; Gimzewski, J. K. Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2007, 2, 780–783.Google Scholar
  60. [60]
    Plodinec, M.; Loparic, M.; Monnier, C. A.; Obermann, E. C.; Zanetti- Dallenbach, R.; Oertle, P.; Hyotyla, J. T.; Aebi, U.; Bentires-Alj, M.; Lim, R. Y. H. et al. The nanomechanical signature of breast cancer. Nat. Nanotechnol. 2012, 7, 757–765.Google Scholar
  61. [61]
    Tian, M. X.; Li, Y. R.; Liu, W. R.; Jin, L.; Jiang, X. F.; Wang, X. Y.; Ding, Z. B.; Peng, Y. F.; Zhou, J.; Fan, J. et al. The nanomechanical signature of liver cancer tissues and its molecular origin. Nanoscale 2015, 7, 12998–13010.Google Scholar
  62. [62]
    Ciasca, G.; Sassun, T. E.; Minelli, E.; Antonelli, M.; Papi, M.; Santoro, A.; Giangaspero, F.; Delfini, R.; De Spirito, M. Nano-mechanical signature of brain tumours. Nanoscale 2016, 8, 19629–19643.Google Scholar
  63. [63]
    Rianna, C.; Radmacher, M. Comparison of viscoelastic properties of cancer and normal thyroid cells on different stiffness substrates. Eur. Biophys. J. 2017, 46, 309–324.Google Scholar
  64. [64]
    Rosales, A. M.; Anseth, K. S. The design of reversible hydrogels to capture extracellular matrix dynamics. Nat. Rev. Mater. 2016, 1, 15012.Google Scholar
  65. [65]
    Ye, K.; Wang, X.; Cao, L. P.; Li, S. Y.; Li, Z. H.; Yu, L.; Ding, J. D. Matrix stiffness and nanoscale spatial organization of cell-adhesive ligands direct stem cell fate. Nano Lett. 2015, 15, 4720–4729.Google Scholar
  66. [66]
    Chaudhuri, P. K.; Low, B. C.; Lim, C. T. Mechanobiology of tumor growth. Chem. Rev. 2018, 118, 6499–6515.Google Scholar
  67. [67]
    Hoshiba, T. Cultured cell-derived decellularized matrices: A review towards the next decade. J. Mater. Chem. B 2017, 5, 4322–4331.Google Scholar
  68. [68]
    Hoshiba, T.; Lu, H. X.; Kawazoe, N.; Chen, G. P. Decellularized matrices for tissue engineering. Expert Opin. Biol. Ther. 2010, 10, 1717–1728.Google Scholar
  69. [69]
    Andreu, I.; Luque, T.; Sancho, A.; Pelacho, B.; Iglesias-García, O.; Melo, E.; Farré, R.; Prósper, F.; Elizalde, M. R.; Navajas, D. Heterogeneous micromechanical properties of the extracellular matrix in healthy and infarcted hearts. Acta Biomater. 2014, 10, 3235–3242.Google Scholar
  70. [70]
    Jorba, I.; Uriarte, J. J.; Campillo, N.; Farré, R.; Navajas, D. Probing micromechanical properties of the extracellular matrix of soft tissues by atomic force microscopy. J. Cell. Physiol. 2017, 232, 19–26.Google Scholar
  71. [71]
    Rianna, C.; Kumar, P.; Radmacher, M. The role of the microenvironment in the biophysics of cancer. Semin. Cell Dev. Biol. 2018, 73, 107–114.Google Scholar
  72. [72]
    Dufrêne, Y. F.; Martínez-Martín, D.; Medalsy, I.; Alsteens, D.; Müller, D. J. Multiparametric imaging of biological systems by force-distance curve-based AFM. Nat. Methods 2013, 10, 847–854.Google Scholar
  73. [73]
    Pfreundschuh, M.; Martinez-Martin, D.; Mulvihill, E.; Wegmann, S.; Muller, D. J. Multiparametric high-resolution imaging of native proteins by forcedistance curve-based AFM. Nat. Protoc. 2014, 9, 1113–1130.Google Scholar
  74. [74]
    Calzado-Martín, A.; Encinar, M.; Tamayo, J.; Calleja, M.; San Paulo, A. Effect of actin organization on the stiffness of living breast cancer cells revealed by peak-force modulation atomic force microscopy. ACS Nano 2016, 10, 3365–3374.Google Scholar
  75. [75]
    Li, Q. S.; Lee, G. Y. H.; Ong, C. N.; Lim, C. T. AFM indentation study of breast cancer cells. Biochem. Biophys. Res. Commun. 2008, 374, 609–613.Google Scholar
  76. [76]
    Heu, C.; Berquand, A.; Elie-Caille, C.; Nicod, L. Glyphosate-induced stiffening of HaCaT keratinocytes, a peak force tapping study on living cells. J. Struct. Biol. 2012, 178, 1–7.Google Scholar
  77. [77]
    Meng, X. H.; Zhang, H.; Song, J. M.; Fan, X. J.; Sun, L. N.; Xie, H. Broad modulus range nanomechanical mapping by magnetic-drive soft probes. Nat. Commun. 2017, 8, 1944.Google Scholar
  78. [78]
    Joo, H. S.; Otto, M. Molecular basis of in vivo biofilm formation by bacterial pathogens. Chem. Biol. 2012, 19, 1503–1513.Google Scholar
  79. [79]
    Decker, R.; Burdelski, C.; Zobiak, M.; Büttner, H.; Franke, G.; Christner, M.; Saβ, K.; Zobiak, B.; Henke, H. A.; Horswill, A. R. et al. An 18 kDa scaffold protein is critical for Staphylococcus epidermidis biofilm formation. PLoS Pathog. 2015, 11, e1004735.Google Scholar
  80. [80]
    Bui, L. M. G.; Conlon, B. P.; Kidd, S. P. Antibiotic tolerance and the alternative lifestyles of Staphylococcus aureus. Essays Biochem. 2017, 61, 71–79.Google Scholar
  81. [81]
    Arciola, C. R.; Campoccia, D.; Montanaro, L. Implant infections: Adhesion, biofilm formation and immune evasion. Nat. Rev. Microbiol. 2018, 16, 397–409.Google Scholar
  82. [82]
    Kong, E. F.; Tsui, C.; Kucharíková, S.; Andes, D.; Van Dijck, P.; Jabra-Rizk, M. A. Commensal protection of Staphylococcus aureus against antimicrobials by candida albicans biofilm matrix. mBio 2016, 7, e01365–16.Google Scholar
  83. [83]
    Ramirez Granillo, A.; Canales, M. G. M.; Espíndola, M. E. S.; Martínez Rivera, M. A.; de Lucio, V. M. B.; Tovar, A. V. R. Antibiosis interaction of Staphylococcus aureus on Aspergillus fumigatus assessed in vitro by mixed biofilm formation. BMC Microbiol. 2015, 15, 33.Google Scholar
  84. [84]
    Beaussart, A.; El-Kirat-Chatel, S.; Herman, P.; Alsteens, D.; Mahillon, J.; Hols, P.; Dufrêne, Y. F. Single-cell force spectroscopy of probiotic bacteria. Biophys. J. 2013, 104, 1886–1892.Google Scholar
  85. [85]
    Herman, P.; Ei-Kirat-Chatel, S.; Beaussart, A.; Geoghegan, J. A.; Vanzieleghem, T.; Foster, T. J.; Hols, P.; Mahillo, J.; Dufrêne, Y. F. Forces driving the attachment of Staphylococcus epidermidis to fibrinogen-coated surfaces. Langmuir 2013, 29, 13018–13022.Google Scholar
  86. [86]
    Formosa-Dague, C.; Feuillie, C.; Beaussart, A.; Derclaye, S.; Kucharíková, S.; Lasa, I.; Van Dijck, P.; Dufrêne, Y. F. Sticky matrix: Adhesion mechanism of the staphylococcal polysaccharide intercellular adhesin. ACS Nano 2016, 10, 3443–3452.Google Scholar
  87. [87]
    Formosa-Dague, C.; Speziale, P.; Foster, T. J.; Geoghegan, J. A.; Dufrêne, Y. F. Zinc-dependent mechanical properties of Staphylococcus aureus biofilm-forming surface protein SasG. Proc. Natl. Acad. Sci. USA 2016, 113, 410–415.Google Scholar
  88. [88]
    Feuillie, C.; Formosa-Dague, C.; Hays, L. M. C.; Vervaeck, O.; Derclaye, S.; Brennan, M. P.; Foster, T. J.; Geoghegan, J. A.; Dufrêne, Y. F. Molecular interactions and inhibition of the staphylococcal biofilm-forming protein SdrC. Proc. Natl. Acad. Sci. USA 2017, 114, 3738–3743.Google Scholar
  89. [89]
    Prystopiuk, V.; Feuillie, C.; Herman-Bausier, P.; Viela, F.; Alsteens, D.; Pietrocola, G.; Speziale, P.; Dufrêne, Y. F. Mechanical forces guiding Staphylococcus aureus cellular invasion. ACS Nano 2018, 12, 3609–3622.Google Scholar
  90. [90]
    Strohmeyer, N.; Bharadwaj, M.; Costell, M.; Fassler, R.; Müller, D. J. Fibronectin-bound a5β1 integrins sense load and signal to reinforce adhesion in less than a second. Nat. Mater. 2017, 16, 1262–1270.Google Scholar
  91. [91]
    Bharadwaj, M.; Strohmeyer, N.; Colo, G. P.; Helenius, J.; Beerenwinkel, N.; Schiller, H. B.; Fässler, R.; Müller, D. J. aV-class integrins exert dual roles on a5β1 integrins to strengthen adhesion to fibronectin. Nat. Commun. 2017, 8, 14348.Google Scholar
  92. [92]
    Sankaran, S.; Jaatinen, L.; Brinkmann, J.; Zambelli, T.; Vörös, J.; Jonkheijm, P. Cell adhesion on dynamic supramolecular surfaces probed by fluid force microscopy-based single-cell force spectroscopy. ACS Nano 2017, 11, 3867–3874.Google Scholar
  93. [93]
    Malek-Zietek, K. E.; Targosz-Korecka, M.; Szymonski, M. The impact of hyperglycemia on adhesion between endothelial and cancer cells revealed by single-cell force spectroscopy. J. Mol. Recognit. 2017, 30, e2628.Google Scholar
  94. [94]
    Smolyakov, G.; Thiebot, B.; Campillo, C.; Labdi, S.; Severac, C.; Pelta, J.; Dague, E. Elasticity, adhesion, and tether extrusion on breast cancer cells provide a signature of their invasive potential. ACS Appl. Mater. Interfaces 2016, 8, 27426–27431.Google Scholar
  95. [95]
    Akanuma, T.; Chen, C.; Sato, T.; Merks, R. M.; Sato, T. N. Memory of cell shape biases stochastic fate decision-making despite mitotic rounding. Nat. Commun. 2016, 7, 11963.Google Scholar
  96. [96]
    Good, M. C.; Vahey, M. D.; Skandarajah, A.; Fletcher, D. A.; Heald, R. Cytoplasmic volume modulates spindle size during embryogenesis. Science 2013, 342, 856–860.Google Scholar
  97. [97]
    Stewart, M. P.; Hodel, A. W.; Spielhofer, A.; Cattin, C. J.; Müller, D. J.; Helenius, J. Wedged AFM-cantilevers for parallel plate cell mechanics. Methods 2013, 60, 186–194.Google Scholar
  98. [98]
    Cattin, C. J.; Düggelin, M.; Martinez-Martin, D.; Gerber, C.; Müller, D. J.; Stewart, M. P. Mechanical control of mitotic progression in single animal cells. Proc. Natl. Acad. Sci. USA 2015, 112, 11258–11263.Google Scholar
  99. [99]
    Stewart, M. P.; Helenius, J.; Toyoda, Y.; Ramanathan, S. P.; Muller, D. J.; Hyman, A. A. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 2011, 469, 226–230.Google Scholar
  100. [100]
    Martínez-Martín, D.; Fläschner, G.; Gaub, B.; Martin, S.; Newton, R.; Beerli, C.; Mercer, J.; Gerber, C.; Müller, D. J. Inertial picobalance reveals fast mass fluctuations in mammalian cells. Nature 2017, 550, 500–505.Google Scholar
  101. [101]
    Prass, M.; Jacobson, K.; Mogilner, A.; Radmacher, M. Direct measurement of the lamellipodial protrusive force in a migrating cell. J. Cell Biol. 2006, 174, 767–772.Google Scholar
  102. [102]
    Longo, G.; Alonso-Sarduy, L.; Rio, L. M.; Bizzini, A.; Trampuz, A.; Notz, J.; Dietler, G.; Kasas, S. Rapid detection of bacterial resistance to antibiotics using AFM cantilevers as nanomechanical sensors. Nat. Nanotechnol. 2013, 8, 522–526.Google Scholar
  103. [103]
    Meister, A.; Gabi, M.; Behr, P.; Studer, P.; Vörös, J.; Niedermann, P.; Bitterli, J.; Polesel-Maris, J.; Liley, M.; Heinzelmann, H. et al. FluidFM: Combining atomic force microscopy and nanofluidics in a universal liquid delivery system for single cell applications and beyond. Nano Lett. 2009, 9, 2501–2507.Google Scholar
  104. [104]
    Guillaume-Gentil, O.; Potthoff, E.; Ossola, D.; Franz, C. M.; Zambelli, T.; Vorholt, J. A. Force-controlled manipulation of single cells: From AFM to FluidFM. Trends Biotechnol. 2014, 32, 381–388.Google Scholar
  105. [105]
    Guillaume-Gentil, O.; Zambelli, T.; Vorholt, J. A. Isolation of single mammalian cells from adherent cultures by fluidic force microscopy. Lab Chip 2014, 14, 402–414.Google Scholar
  106. [106]
    Guillaume-Gentil, O.; Grindberg, R. V.; Kooger, R.; Dorwling-Carter, L.; Martinez, V.; Ossola, D.; Pilhofer, M.; Zambelli, T.; Vorholt, J. A. Tunable single-cell extraction for molecular analyses. Cell 2016, 166, 506–516.Google Scholar
  107. [107]
    Guillaume-Gentil, O.; Rey, T.; Kiefer, P.; Ibáñez, A. J.; Steinhoff, R.; Bronnimann, R.; Dorwling-Carter, L.; Zambelli, T.; Zenobi, R.; Vorholt, J. A. Single-cell mass Spectrometry of metabolites extracted from live cells by fluidic force microscopy. Anal. Chem. 2017, 89, 5017–5023.Google Scholar
  108. [108]
    Ossola, D.; Amarouch, M. Y.; Behr, P.; Vörös, J.; Abriel, H.; Zambelli, T. Force-controlled patch clamp of beating cardiac cells. Nano Lett. 2015, 15, 1743–1750.Google Scholar
  109. [109]
    Li, G. Y.; Xi, N.; Yu, M. M.; Fung, W. K. Development of augmented reality system for AFM-based nanomanipulation. IEEE/ASME Trans. Mech. 2004, 9, 358–365.Google Scholar
  110. [110]
    Song, B.; Yang, R. G.; Xi, N.; Patterson, K. C.; Qu, C. G.; Lai, K. W. C. Cellular-level surgery using nano robots. J. Lab. Autom. 2012, 17, 425–434.Google Scholar
  111. [111]
    Li, G. Y.; Xi, N.; Wang, D. H. In situ sensing and manipulation of molecules in biological samples using a nanorobotic system. Nanomedicine 2005, 1, 31–40.Google Scholar
  112. [112]
    Yang, R. G.; Song, B.; Sun, Z. Y.; Lai, K. W.; Fung, C. K. M.; Patterson, K. C.; Seiffert-Sinha, K.; Sinha, A. A.; Xi, N. Cellular level robotic surgery: Nanodissection of intermediate filaments in live keratinocytes. Nanomedicine 2015, 11, 137–145.Google Scholar
  113. [113]
    Zhang, C. L.; Li, P.; Liu, L. Q.; Wang, Y. C.; Gao, Z. B.; Li, G. Y. Development of mechanostimulated patch-clamp system for cellular physiological study. IEEE/ASME Trans. Mech. 2014, 19, 1138–1147.Google Scholar
  114. [114]
    Yang, Y. L.; Yu, J.; Monemian Esfahani, A.; Seiffert-Sinha, K.; Xi, N.; Lee, I.; Sinha, A. A.; Chen, L. L.; Sun, Z. Y.; Yang, R. G. et al. Single-cell membrane drug delivery using porous pen nanodeposition. Nanoscale 2018, 10, 12704–12712.Google Scholar
  115. [115]
    Xie, H.; Haliyo, D. S.; Regnier, S. Parallel imaging/manipulation force microscopy. Appl. Phys. Lett. 2009, 94, 153106.Google Scholar
  116. [116]
    Xie, H.; Yin, M. N.; Rong, W. B.; Sun, L. N. In situ quantification of living cell adhesion forces: Single cell force spectroscopy with a nanotweezer. Langmuir 2014, 30, 2952–2959.Google Scholar
  117. [117]
    Müller, D. J.; Helenius, J.; Alsteens, D.; Dufrêne, Y. F. Force probing surfaces of living cells to molecular resolution. Nat. Chem. Biol. 2009, 5, 383–390.Google Scholar
  118. [118]
    Dufrêne, Y. F. Sticky microbes: Forces in microbial cell adhesion. Trends Microbiol. 2015, 23, 376–382.Google Scholar
  119. [119]
    Chaudhuri, O.; Parekh, S. H.; Lam, W. A.; Fletcher, D. A. Combined atomic force microscopy and side-view optical imaging for mechanical studies of cells. Nat. Methods 2009, 6, 383–387.Google Scholar
  120. [120]
    Lam, W. A.; Chaudhuri, O.; Crow, A.; Webster, K. D.; Li, T. D.; Kita, A.; Huang, J.; Fletcher, D. A. Mechanics and contraction dynamics of single platelets and implications for clot stiffening. Nat. Mater. 2011, 10, 61–66.Google Scholar
  121. [121]
    Moeendarbary, E.; Valon, L.; Fritzsche, M.; Harris, A. R.; Moulding, D. A.; Thrasher, A. J.; Stride, E.; Mahadevan, L.; Charras, G. T. The cytoplasm of living cells behaves as a poroelastic material. Nat. Mater. 2013, 12, 253–261.Google Scholar
  122. [122]
    Shen, Y. J.; Nakajima, M.; Zhang, Z. H.; Fukuda, T. Dynamic force characterization microscopy based on integrated nanorobotic AFM and SEM system for detachment process study. IEEE/ASME Trans. Mech. 2015, 20, 3009–3017.Google Scholar
  123. [123]
    Shen, Y. J.; Nakajima, M.; Yang, Z.; Tajima, H.; Najdovski, Z.; Homma, M.; Fukuda, T. Single cell stiffness measurement at various humidity conditions by nanomanipulation of a nano-needle. Nanotechnology 2013, 24, 145703.Google Scholar
  124. [124]
    Ahmad, M. R.; Nakajima, M.; Kojima, S.; Homma, M.; Fukuda, T. Nanoindentation methods to measure viscoelastic properties of single cells using sharp, flat, and buckling tips inside ESEM. IEEE Trans. Nanobiosci. 2010, 9, 12–23.Google Scholar
  125. [125]
    Li, M.; Liu, L. Q.; Xi, N.; Wang, Y. C.; Xiao, X. B.; Zhang, W. J. Effects of temperature and cellular interactions on the mechanics and morphology of human cancer cells investigated by atomic force microscopy. Sci. China Life Sci. 2015, 58, 889–901.Google Scholar
  126. [126]
    Mari, S. A.; Pessoa, J.; Altieri, S.; Hensen, U.; Thomas, L.; Morais-Cabral, J. H.; Müller, D. J. Gating of the MlotiK1 potassium channel involves large rearrangements of the cyclic nucleotide-binding domains. Proc. Natl. Acad. Sci. USA 2011, 108, 20802–20807.Google Scholar
  127. [127]
    Laskowski, P. R.; Pfreundschuh, M.; Stauffer, M.; Ucurum, Z.; Fotiadis, D.; Müller, D. J. High-resolution imaging and multiparametric characterization of native membranes by combining confocal microscopy and an atomic force microscopy-based toolbox. ACS Nano 2017, 11, 8292–8301.Google Scholar
  128. [128]
    Müller, D. J.; Dufrêne, Y. F. Atomic force microscopy: A nanoscopic window on the cell surface. Trends Cell Biol. 2011, 21, 461–469.Google Scholar
  129. [129]
    Hochmuth, R. M.; Evans, C. A.; Wiles, H. C.; McCown, J. T. Mechanical measurement of red cell membrane thickness. Science 1983, 220, 101–102.Google Scholar
  130. [130]
    Casuso, I.; Khao, J.; Chami, M.; Paul-Gilloteaux, P.; Husain, M.; Duneau, J. P.; Stahlberg, H.; Sturgis, J. N.; Scheuring, S. Characterization of the motion of membrane proteins using high-speed atomic force microscopy. Nat. Nanotechnol. 2012, 7, 525–529.Google Scholar
  131. [131]
    Ewald, A. J.; Egeblad, M. Cancer: Sugar-coated cell signalling. Nature 2014, 511, 298–299.Google Scholar
  132. [132]
    Dumitru, A. C.; Poncin, M. A.; Conrard, L.; Dufrêne, Y. F.; Tyteca, D.; Alsteens, D. Nanoscale membrane architecture of healthy and pathological red blood cells. Nanoscale Horiz. 2018, 3, 293–304.Google Scholar
  133. [133]
    Ando, T.; Uchihashi, T.; Kodera, N. High-speed AFM and applications to biomolecular systems. Annu. Rev. Biophys. 2013, 42, 393–414.Google Scholar
  134. [134]
    Watanabe, S.; Ando, T. High-speed XYZ-nanopositioner for scanning ion conductance microscopy. Appl. Phys. Lett. 2017, 111, 113106.Google Scholar
  135. [135]
    Ando, T. High-speed atomic force microscopy and its future prospects. Biophys. Rev. 2018, 10, 285–292.Google Scholar
  136. [136]
    Cai, M. J.; Zhao, W. D.; Shang, X.; Jiang, J. G.; Ji, H. B.; Tang, Z. Y.; Wang, H. D. Direct evidence of lipid rafts by in situ atomic force microscopy. Small 2012, 8, 1243–1250.Google Scholar
  137. [137]
    Alsteens, D.; Newton, R.; Schubert, R.; Martinez-Martin, D.; Delguste, M.; Roska, B.; Müller, D. J. Nanomechanical mapping of first binding steps of a virus to animal cells. Nat. Nanotechnol. 2017, 12, 177–183.Google Scholar
  138. [138]
    Li, M.; Liu, L. Q.; Xi, N.; Wang, Y. C. Applications of micro/nano automation technology in detecting cancer cells for personalized medicine. IEEE Trans. Nanotechnol. 2017, 16, 217–229.Google Scholar
  139. [139]
    Wang, Z. B.; Liu, L. Q.; Wang, Y. C.; Xi, N.; Dong, Z. L.; Li, M.; Yuan, S. A fully automated system for measuring cellular mechanical properties. J. Lab. Autom. 2012, 17, 443–448.Google Scholar
  140. [140]
    Alsteens, D.; Müller, D. J.; Dufrêne, Y. F. Multiparametric atomic force microscopy imaging of biomolecular and cellular systems. Acc. Chem. Res. 2017, 50, 924–931.Google Scholar
  141. [141]
    Galluzzi, M.; Tang, G. L.; Biswas, C. S.; Zhao, J. L.; Chen, S. G.; Stadler, F. J. Atomic force microscopy methodology and AFMech suite software for nanomechanics on heterogeneous soft materials. Nat. Commun. 2018, 9, 3584.Google Scholar
  142. [142]
    Yu, H. M.; Mouw, J. K.; Weaver, V. M. Forcing form and function: Biomechanical regulation of tumor evolution. Trends Cell Biol. 2011, 21, 47–56.Google Scholar
  143. [143]
    Butt, H. J.; Cappela, B.; Kappl, M. Force measurements with the atomic force microscope: Technique, interpretation and applications. Surf. Sci. Rep. 2005, 59, 1–152.Google Scholar
  144. [144]
    Gavara, N. Combined strategies for optimal detection of the contact point in AFM force-indentation curves obtained on thin samples and adherent cells. Sci. Rep. 2016, 6, 21267.Google Scholar
  145. [145]
    Li, M.; Dang, D.; Liu, L. Q.; Xi, N.; Wang, Y. C. Atomic force microscopy in characterizing cell mechanics for biomedical applications: A review. IEEE Trans. Nanobiosci. 2017, 16, 523–540.Google Scholar
  146. [146]
    Churnside, A. B.; Sullan, R. M. A.; Nguyen, D. M.; Case, S. O.; Bull, M. S.; King, G. M.; Perkins, T. T. Routine and timely sub-piconewton force stability and precision for biological applications of atomic force microscopy. Nano Lett. 2012, 12, 3557–3561.Google Scholar
  147. [147]
    Dufrêne, Y. F.; Evans, E.; Engel, A.; Helenius, J.; Gaub, H. E.; Müller, D. J. Five challenges to bringing single-molecule force spectroscopy into living cells. Nat. Methods 2011, 8, 123–127.Google Scholar
  148. [148]
    Schillers, H.; Rianna, C.; Schäpe, J.; Luque, T.; Doschke, H.; Wälte, M.; Uriarte, J. J.; Campillo, N.; Michanetzis, G. P. A.; Bobrowska, J. et al. Standardized nanomechanical atomic force microscopy procedure (SNAP) for measuring soft and biological samples. Sci. Rep. 2017, 7, 5117.Google Scholar
  149. [149]
    Yu, W. B.; Sharma, S.; Gimzewski, J. K.; Rao, J. Y. Nanocytology as a potential biomarker for cancer. Biomark. Med. 2017, 11, 213–216.Google Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Robotics, Shenyang Institute of AutomationChinese Academy of SciencesShenyangChina
  2. 2.Institutes for Robotics and Intelligent ManufacturingChinese Academy of SciencesShenyangChina
  3. 3.Department of Industrial and Manufacturing Systems EngineeringThe University of Hong KongHong KongChina

Personalised recommendations