Skip to main content

Advertisement

SpringerLink
Log in

Depth-sensing analysis of cytoskeleton organization based on AFM data

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

Atomic force microscopy is a common technique used to determine the elastic properties of living cells. It furnishes the relative Young’s modulus, which is typically determined for indentation depths within the range 300–500 nm. Here, we present the results of depth-sensing analysis of the mechanical properties of living fibroblasts measured under physiological conditions. Distributions of the Young’s moduli were obtained for all studied cells and for every cell. The results show that for small indentation depths, histograms of the relative values of the Young’s modulus described the regions rich in the network of actin filaments. For large indentation depths, the overall stiffness of a whole cell was obtained, which was accompanied by a decrease of the modulus value. In conclusion, the results enable us to describe the non-homogeneity of the cell cytoskeleton, particularly, its contribution linked to actin filaments located beneath the cell membrane. Preliminary results showing a potential application to improve the detection of cancerous cells, have been presented for melanoma cell lines.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AFM:

Atomic force microscopy

MEM:

Minimum essential medium

EDTA:

Ethylenediaminetetraacetic acid

PBS:

Phosphate-buffered saline

FWHH:

Full width of the distribution taken at half height

References

  • Canadas P, Laurent V, Oddou C, Isabey D, Wendling S (2002) A cellular tensegrity model to analyse the structural viscoelasticity of the cytoskeleton. J Theor Biol 218:155–173

    Article  PubMed  Google Scholar 

  • Cross SE, Jin YS, Tondre J, Wong R, Rao J, Gimzewski JK (2008) AFM-based analysis of human metastatic cancer cells. Nanotechnology 19:384003

    Article  PubMed  Google Scholar 

  • Cuerrier CM, Gagner A, Lebel R, Gobeil F, Grandbois M (2009) Effect of thrombin and bradykinin on endothelial cell mechanical properties monitored through membrane deformation. J Mol Recognit 22:389–396

    Article  PubMed  CAS  Google Scholar 

  • DeMali KA, Wennerberg K, Burridge K (2003) Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol 15:572–582

    Article  PubMed  CAS  Google Scholar 

  • Discher D, Dong C, Fredberg JJ, Guilak F, Ingber D, Janmey P, Kamm RD, Schmid-Schoenbein GW, Weinbaum S (2009) Biomechanics: cell research and applications for the next decade. Ann Biomed Eng 37:847–859

    Article  PubMed  Google Scholar 

  • Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, Tello M, Osteo-Ibanez T, Pellinen T, Echarri A, Cerezo A, Klein-Szanto AJP, Garcia R, Kelly PJ, Sanchez-Mateo P, Cukierman E, Del Pozo MA (2011) Biomechanical remodelling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 146:148–163

    Article  PubMed  CAS  Google Scholar 

  • Guck J, Schinkinger S, Lincoln B, Wottawah F, Ebert S, Romeyke M, Lenz D, Erickson HM, Ananthakrishnan R, Mitchell D, Käs J, Ulvick S, Bilby S (2005) Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys J 88:3689–3698

    Article  PubMed  CAS  Google Scholar 

  • Haidle AM, Myers AG (2004) An enantioselective, modular, and general route to the cytochalasins: synthesis of L-696, 474 and cytochalasin B. Proc Natl Acad Sci 101:12048–12053

    Article  PubMed  CAS  Google Scholar 

  • Lekka M, Laidler P (2009) Applicability of AFM in cancer detection. Nat Nanotech (correspondence) 4:72

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lekka M, Laidler P, Ignacak J, Łabędź M, Lekki J, Struszczyk H, Stachura Z, Hrynkiewicz AZ (2001) The effect of chitosan on stiffness and glycolytic activity of human bladder cells. Biochim Biophys Acta 1540:127–136

    Article  PubMed  CAS  Google Scholar 

  • Li QS, Lee GYH, Ong CN, Lim CT (2008) AFM indentation study of breast cancer cells. Biochem Biophys Res Commun 374:609–613

    Article  PubMed  CAS  Google Scholar 

  • Liu W, Fan Y, Deng X, Guan Z, Li N (2009) Adhesion behaviors of human trophoblast cells by contact with endothelial cells. Colloid Surf B 71:208–213

    Article  CAS  Google Scholar 

  • Pesen D, Hoh HJ (2005) Micromechanical architecture of the endothelial cell cortex. Biophys J 88:670–679

    Article  PubMed  CAS  Google Scholar 

  • Remmerbach TW, Wottawah F, Dietrich J, Lincoln B, Wittekind C, Guck J (2009) Oral cancer diagnosis by mechanical phenotyping. Cancer Res 69:1728–1732

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Safran S, Gov N, Nicolas A, Schwarz U, Tlusty T (2005) Physics of cell elasticity, shape and adhesion. Phys A 352:171–201

    Article  CAS  Google Scholar 

  • Schrot S, Weidenfeller C, Schaffer TE, Robenek H, Galla HJ (2005) Influence of hydrocortisone on the mechanical properties of the cerebral endothelium in vitro. Biophys J 89:3904–3910

    Article  PubMed  CAS  Google Scholar 

  • Seo Y, Jhe W (2008) Atomic force microscopy and spectroscopy. Rep Prog Phys 71:016101

    Article  Google Scholar 

  • Sneddon IA (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

    Article  Google Scholar 

  • Suresh S (2007) Biomechanics and biophysics of cancer cells. Acta Biomater 3:413–438

    Article  PubMed  Google Scholar 

  • Wakatsuki T, Schwab B, Thompson N, Elson E (2001) Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J Cell Sci 114:1025–1036

    PubMed  CAS  Google Scholar 

  • Weichsel J, Herold N, Lehmann MJ, Kraeusslich HG, Schwarz US (2010) A quantitative measure for alterations in the actin cytoskeleton investigated with automated high-throughput microscopy. Cytometry A 77:52–63

    PubMed  Google Scholar 

  • Wu WH, Kuhn T, Moy VT (1998) Mechanical properties of L929 cells measured by atomic force microscopy: effects of anticytoskeletal drugs and membrane crosslinking. Scanning 20:389–397

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi H, Condeelis J (2007) Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta 1773:642–652

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Giannakakou P (2005) Targeting microtubules for cancer chemotherapy. Curr Med Chem 5:65–71

    CAS  Google Scholar 

  • Zhu C, Bao G, Wang N (2000) Cell mechanics: mechanical response, cell adhesion, and molecular deformation. Annu Rev Biomed Eng 2:189–226

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was partially supported by the project SMW (Single Molecule Workstation), grant agreement number 213717 (NMP4-SE-2008-213717), and by the projects of the Polish Ministry of Science and Higher Education numbers: N-N202-285738 (O.K.) and N-N402-47133 (M.F.).

Author information

Authors and Affiliations

  1. The Henryk Niewodniczański Institute of Nuclear Physics, Polish Academy of Sciences, Radzikowskiego 152, 31-342, Kraków, Poland

    Katarzyna Pogoda, Justyna Jaczewska, Joanna Wiltowska-Zuber, Olesya Klymenko, Kazimierz Zuber & Małgorzata Lekka

  2. The Smoluchowski Institute of Physics, Jagiellonian University, Reymonta 4, 30-059, Kraków, Poland

    Justyna Jaczewska

  3. The Department of Internal Medicine and Gerontology, Collegium Medicum, Jagiellonian University, Śniadeckich 10, Kraków, Poland

    Maria Fornal

Authors
  1. Katarzyna Pogoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Justyna Jaczewska
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joanna Wiltowska-Zuber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Olesya Klymenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kazimierz Zuber
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Fornal
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Małgorzata Lekka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Małgorzata Lekka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pogoda, K., Jaczewska, J., Wiltowska-Zuber, J. et al. Depth-sensing analysis of cytoskeleton organization based on AFM data. Eur Biophys J 41, 79–87 (2012). https://doi.org/10.1007/s00249-011-0761-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-011-0761-9

Keywords

Search

Navigation