Skip to main content

In Situ Measuring Mechanical Properties of Normal and Disease Cells

  • Chapter
  • First Online:
Atomic Force Microscopy in Molecular and Cell Biology

Abstract

Atomic force microscopy (AFM) has recently made great progress in mapping local mechanical properties of a single cell including living cell. These mechanical properties can provide not only cellular nano- and micro-structure, but also physiological and pathological information of cells. Here, the recent applications of AFM for the study of mechanical characteristics of normal cells and disease cells are reviewed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Montell DJ. Morphogenetic cell movements: diversity from modular mechanical properties. Science. 2008;322:1502–5.

    Article  CAS  Google Scholar 

  2. Guedes AF, Carvalho FA, Malho I, Lousada N, Sargento L, Santos NC. Atomic force microscopy as a tool to evaluate the risk of cardiovascular diseases in patients. Nat Nanotechnol. 2016;11:687–92.

    Article  CAS  Google Scholar 

  3. Gardel ML, Schneider IC, Aratyn-Schaus Y, Waterman CM. Mechanical integration of actin and adhesion dynamics in cell migration. In: Schekman R, Goldstein L, Lehmann R, editors. Annual review of cell and developmental biology, vol. 26. Palo Alto: Annual Reviews; 2010. p. 315–33.

    Google Scholar 

  4. Chen W, Zhu C. Mechanical regulation of T-cell functions. Immunol Rev. 2013;256:160–76.

    Article  CAS  Google Scholar 

  5. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310:1139–43.

    Article  CAS  Google Scholar 

  6. Parsons JT, Horwitz AR, Schwartz MA. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol. 2010;11:633–43.

    Article  CAS  Google Scholar 

  7. Zhang GC, Fan N, Lv XY, Liu YY, Guo J, Yang LX, et al. Investigation of the mechanical properties of the human osteosarcoma cell at different cell cycle stages. Micromachines. 2017;8.

    Google Scholar 

  8. Fletcher DA, Mullins D. Cell mechanics and the cytoskeleton. Nature. 2010;463:485–92.

    Article  CAS  Google Scholar 

  9. Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell. 2011;147:992–1009.

    Article  CAS  Google Scholar 

  10. Schroeder MC, Halder G. Regulation of the hippo pathway by cell architecture and mechanical signals. Semin Cell Dev Biol. 2012;23:803–11.

    Article  CAS  Google Scholar 

  11. Hoffman BD, Grashoff C, Schwartz MA. Dynamic molecular processes mediate cellular mechanotransduction. Nature. 2011;475:316–23.

    Article  CAS  Google Scholar 

  12. Mierke CT. The fundamental role of mechanical properties in the progression of cancer disease and inflammation. Rep Prog Phys. 2014;77:076602.

    Article  Google Scholar 

  13. Hu HY, Candiello J, Zhang P, Ball SL, Cameron DA, Halfter W. Retinal ectopias and mechanically weakened basement membrane in a mouse model of muscle-eye-brain (MEB) disease congenital muscular dystrophy. Mol Vis. 2010;16:1415–28.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Humphrey JD, Dufresne ER, Schwartz MA. Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol. 2014;15:802–12.

    Article  CAS  Google Scholar 

  15. Patel NR, Bole M, Chen C, Hardin CC, Kho AT, Mih J, et al. Cell elasticity determines macrophage function. PLoS One. 2012;7:e41024.

    Article  CAS  Google Scholar 

  16. Muller DJ, Dufrene YF. Atomic force microscopy: a nanoscopic window on the cell surface. Trends Cell Biol. 2011;21:461–9.

    Article  Google Scholar 

  17. Dufrene YF, Ando T, Garcia R, Alsteens D, Martinez-Martin D, Engel A, et al. Imaging modes of atomic force microscopy for application in molecular and cell biology. Nat Nanotechnol. 2017;12:295–307.

    Article  CAS  Google Scholar 

  18. Raman A, Trigueros S, Cartagena A, Stevenson APZ, Susilo M, Nauman E, et al. Mapping nanomechanical properties of live cells using multi-harmonic atomic force microscopy. Nat Nanotechnol. 2011;6:809–14.

    Article  CAS  Google Scholar 

  19. Alsteens D, Muller DJ, Dufrene YF. Multiparametric atomic force microscopy imaging of biomolecular and cellular systems. Acc Chem Res. 2017;50:924–31.

    Article  CAS  Google Scholar 

  20. Alsteens D, Beaussart A, El-Kirat-Chatel S, Sullan RMA, Dufrene YF. Atomic force microscopy: a new look at pathogens. PLoS Pathog. 2013;9:e1003516.

    Article  CAS  Google Scholar 

  21. Lekka M, Pogoda K, Gostek J, Klymenko O, Prauzner-Bechcicki S, Wiltowska-Zuber J, et al. Cancer cell recognition - mechanical phenotype. Micron. 2012;43:1259–66.

    Article  Google Scholar 

  22. Plodinec M, Loparic M, Monnier CA, Obermann EC, Zanetti-Dallenbach R, Oertle P, et al. The nanomechanical signature of breast cancer. Nat Nanotechnol. 2012;7:757–65.

    Article  CAS  Google Scholar 

  23. Ansardamavandi A, Tafazzoli-Shadpour M, Omidvar R, Jahanzad I. Quantification of effects of cancer on elastic properties of breast tissue by atomic force microscopy. J Mech Behav Biomed Mater. 2016;60:234–42.

    Article  Google Scholar 

  24. Esbona K, Inman D, Saha S, Jeffery J, Schedin P, Wilke L, et al. COX-2 modulates mammary tumor progression in response to collagen density. Breast Cancer Res. 2016;18:35.

    Article  Google Scholar 

  25. Calzado-Martin A, Encinar M, Tamayo J, Calleja M, Paulo AS. Effect of actin organization on the stiffness of living breast Cancer cells revealed by peak-force modulation atomic force microscopy. ACS Nano. 2016;10:3365–74.

    Article  CAS  Google Scholar 

  26. Li QS, Lee GYH, Ong CN, Lim CT. AFM indentation study of breast cancer cells. Biochem Biophys Res Commun. 2008;374:609–13.

    Article  CAS  Google Scholar 

  27. Dokukin ME, Guz NV, Sokolov I. Mechanical properties of cancer cells depend on number of passages: atomic force microscopy indentation study. Jpn J Appl Phys. 2017;56:08LB01.

    Article  Google Scholar 

  28. Prabhune M, Belge G, Dotzauer A, Bullerdiek J, Radmacher M. Comparison of mechanical properties of normal and malignant thyroid cells. Micron. 2012;43:1267–72.

    Article  Google Scholar 

  29. Xu WW, Mezencev R, Kim B, Wang LJ, Mcdonald J, Sulchek T. Cell stiffness is a biomarker of the metastatic potential of ovarian Cancer cells. PLoS One. 2012;7.

    Article  CAS  Google Scholar 

  30. Quan FS, Kim KS. Medical applications of the intrinsic mechanical properties of single cells. Acta Biochim Biophys Sin. 2016;48:865–71.

    Article  CAS  Google Scholar 

  31. Andolfi L, Bourkoula E, Migliorini E, Palma A, Pucer A, Skrap M, et al. Investigation of adhesion and mechanical properties of human glioma cells by single cell force spectroscopy and atomic force microscopy. PLoS One. 2014;9:e112582.

    Article  Google Scholar 

  32. Le Cigne A, Chieze L, Beaussart A, El-Kirat-Chatel S, Dufrene YF, Dedieu S, et al. Analysis of the effect of LRP-1 silencing on the invasive potential of cancer cells by nanomechanical probing and adhesion force measurements using atomic force microscopy. Nanoscale. 2016;8:7144–54.

    Article  Google Scholar 

  33. Cai X, Gao S, Cai J, Wu Y, Deng H. Artesunate induced morphological and mechanical changes of Jurkat cell studied by AFM. Scanning. 2009;31:83–9.

    Article  CAS  Google Scholar 

  34. Cai X, Xing X, Cai J, Chen Q, Wu S, Huang F. Connection between biomechanics and cytoskeleton structure of lymphocyte and Jurkat cells: an AFM study. Micron. 2010;41:257–62.

    Article  CAS  Google Scholar 

  35. Iyer S, Gaikwad RM, Subba-Rao V, Woodworth CD, Sokolov I. Atomic force microscopy detects differences in the surface brush of normal and cancerous cells. Nat Nanotechnol. 2009;4:389–93.

    Article  CAS  Google Scholar 

  36. Rianna C, Radmacher M. Influence of microenvironment topography and stiffness on the mechanics and motility of normal and cancer renal cells. Nanoscale. 2017;9:11222–30.

    Article  CAS  Google Scholar 

  37. Rianna C, Radmacher M. Comparison of viscoelastic properties of cancer and normal thyroid cells on different stiffness substrates. Eur Biophys J Biophys Lett. 2017;46:309–24.

    Article  CAS  Google Scholar 

  38. Pi J, Jin H, Jiang J, Yang F, Cai H, Yang P, et al. Single molecule force spectroscopy for in-situ probing oridonin inhibited ROS-mediated EGF-EGFR interactions in living KYSE-150 cells. Pharmacol Res. 2017;119:479–89.

    Article  CAS  Google Scholar 

  39. Pi J, Cai H, Jin H, Yang F, Jiang J, Wu A, et al. Qualitative and quantitative analysis of ROS-mediated Oridonin-induced Oesophageal Cancer KYSE-150 cell apoptosis by atomic force microscopy. PLoS One. 2015;10:e0140935.

    Article  Google Scholar 

  40. Zhang L, Yang F, Cai J-Y, Yang P-H, Liang Z-H. In-situ detection of resveratrol inhibition effect on epidermal growth factor receptor of living MCF-7 cells by atomic force microscopy. Biosens Bioelectron. 2014;56:271–7.

    Article  CAS  Google Scholar 

  41. Pi J, Li B, Tu L, Zhu H, Jin H, Yang F, et al. Investigation of quercetin-induced HepG2 cell apoptosis-associated cellular biophysical alterations by atomic force microscopy. Scanning. 2016;38:100–12.

    Article  CAS  Google Scholar 

  42. Wang M, Ruan Y, Xing X, Chen Q, Peng Y, Cai J. Curcumin induced nanoscale CD44 molecular redistribution and antigen-antibody interaction on HepG2 cell surface. Anal Chim Acta. 2011;697:83–9.

    Article  CAS  Google Scholar 

  43. Pi J, Huang L, Yang F, Jiang J, Jin H, Liu J, et al. Atomic force microscopy study of ionomycin-induced degranulation in RBL-2H3 cells. Scanning. 2016;38:525–34.

    Article  CAS  Google Scholar 

  44. Pi J, Li T, Liu J, Su X, Wang R, Yang F, et al. Detection of lipopolysaccharide induced inflammatory responses in RAW264.7 macrophages using atomic force microscope. Micron. 2014;65:1–9.

    Article  CAS  Google Scholar 

  45. Minetti G, Egee S, Morsdorf D, Steffen P, Makhro A, Achilli C, et al. Red cell investigations: art and artefacts. Blood Rev. 2013;27:91–101.

    Article  CAS  Google Scholar 

  46. Szablewski L, Sulima A. The structural and functional changes of blood cells and molecular components in diabetes mellitus. Biol Chem. 2017;398:411–23.

    Article  CAS  Google Scholar 

  47. Greenwood BM, Bojang K, Whitty CJM, Targett GAT. Malaria. Lancet. 2005;365:1487–98.

    Article  CAS  Google Scholar 

  48. Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, Conzelmann C, et al. First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med. 2011;365:1863–75.

    Article  Google Scholar 

  49. Rossi G, De Smet M, Khim N, Kindermans JM, Menard D. Performance of rapid diagnostic testing in patients with suspected malaria in Cambodia, a low-Endemicity country aiming for malaria elimination. Clin Infect Dis. 2017;65:1769–70.

    Article  Google Scholar 

  50. Shi H, Liu Z, Li A, Yin J, Chong AGL, Tan KSW, et al. Life cycle-dependent cytoskeletal modifications in Plasmodium falciparum infected erythrocytes. PLoS One. 2013;8.

    Article  CAS  Google Scholar 

  51. Sinha A, Chu TTT, Dao M, Chandramohanadas R. Single-cell evaluation of red blood cell bio-mechanical and nano-structural alterations upon chemically induced oxidative stress. Sci Rep. 2015;5.

    Google Scholar 

  52. Valle-Delgado JJ, Urban P, Fernandez-Busquets X. Demonstration of specific binding of heparin to Plasmodium falciparum-infected vs non-infected red blood cells by single-molecule force spectroscopy. Nanoscale. 2013;5:3673–80.

    Article  CAS  Google Scholar 

  53. Dulinska I, Targosz M, Strojny W, Lekka M, Czuba P, Balwierz W, et al. Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. J Biochem Biophys Methods. 2006;66:1–11.

    Article  CAS  Google Scholar 

  54. Maciaszek JL, Lykotrafitis G. Sickle cell trait human erythrocytes are significantly stiffer than normal. J Biomech. 2011;44:657–61.

    Article  Google Scholar 

  55. Maciaszek JL, Andemariam B, Lykotrafitis G. Microelasticity of red blood cells in sickle cell disease. J Strain Anal Eng Des. 2011;46:368–79.

    Article  Google Scholar 

  56. Ciasca G, Papi M, Di Claudio S, Chiarpotto M, Palmieri V, Maulucci G, et al. Mapping viscoelastic properties of healthy and pathological red blood cells at the nanoscale level. Nanoscale. 2015;7:17030–7.

    Article  CAS  Google Scholar 

  57. Buys AV, Van Rooy MJ, Soma P, Van Papendorp D, Lipinski B, Pretorius E. Changes in red blood cell membrane structure in type 2 diabetes: a scanning electron and atomic force microscopy study. Cardiovasc Diabetol. 2013;12:25.

    Article  Google Scholar 

  58. Lekka M, Fornal M, Pyka-Fosciak G, Lebed K, Wizner B, Grodzicki T, et al. Erythrocyte stiffness probed using atomic force microscope. Biorheology. 2005;42:307–17.

    PubMed  Google Scholar 

  59. Zhang L, Pi J, Shi Q, Cai J, Yang P, Liang Z. In situ single molecule detection of insulin receptors on erythrocytes from a type 1 diabetes ketoacidosis patient by atomic force microscopy. Analyst. 2015;140:7407–16.

    Article  CAS  Google Scholar 

  60. Li S-P, Xie W-L, Cai H-H, Cai J-Y, Yang P-H. Hydroxyl radical scavenging mechanism of human erythrocytes by quercetin-germanium (IV) complex. Eur J Pharm Sci. 2012;47:28–34.

    Article  Google Scholar 

  61. Kaczmarska M, Fornal M, Messerli FH, Korecki J, Grodzicki T, Burda K. Erythrocyte membrane properties in patients with essential hypertension. Cell Biochem Biophys. 2013;67:1089–102.

    Article  CAS  Google Scholar 

  62. Guedes AF, Carvalho FA, Moreira C, Nogueira JB, Santos NC. Essential arterial hypertension patients present higher cell adhesion forces, contributing to fibrinogen-dependent cardiovascular risk. Nanoscale. 2017;9:14897–906.

    Article  CAS  Google Scholar 

  63. Cluitmans JCA, Hardeman MR, Dinkla S, Brock R, Bosman G. Red blood cell deformability during storage: towards functional proteomics and metabolomics in the blood Bank. Blood Transf. 2012;10:S12–S8.

    Google Scholar 

  64. Girasole M, Dinarelli S, Boumis G. Structural, morphological and nanomechanical characterisation of intermediate states in the ageing of erythrocytes. J Mol Recognit. 2012;25:285–91.

    Article  CAS  Google Scholar 

  65. Kozlova E, Chernysh A, Moroz V, Sergunova V, Gudkova O, Manchenko E. Morphology, membrane nanostructure and stiffness for quality assessment of packed red blood cells. Sci Rep. 2017;7:7846.

    Article  CAS  Google Scholar 

  66. Wang XL, Yang YJ, Hu XH, Kawazoe N, Yang YN, Chen GP. Morphological and mechanical properties of osteosarcoma microenvironment cells explored by atomic force microscopy. Anal Sci. 2016;32:1177–82.

    Article  CAS  Google Scholar 

  67. Jin H, Xing XB, Zhao HX, Chen Y, Huang X, Ma SY, et al. Detection of erythrocytes influenced by aging and type 2 diabetes using atomic force microscope. Biochem Biophys Res Commun. 2010;391:1698–702.

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by Guangdong Natural Science Foundation, China (No. 2016A030313078), the Fundamental Research Funds for the Central Universities, China (No. 21617430), Foundation for Distinguished Young Talents in Higher Education of Guangdong, China (No. LYM11020), and Macau FDCT (No. 028/2014/A1).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sui-Ping Deng or Jiye Cai .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Deng, SP., Yang, YL., Cheng, XX., Li, WR., Cai, J. (2018). In Situ Measuring Mechanical Properties of Normal and Disease Cells. In: Cai, J. (eds) Atomic Force Microscopy in Molecular and Cell Biology. Springer, Singapore. https://doi.org/10.1007/978-981-13-1510-7_9

Download citation

Publish with us

Policies and ethics