Skip to main content
SpringerLink
Log in

Transiently crosslinked F-actin bundles

  • Biophysics Letter
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

F-actin bundles are prominent cytoskeletal structures in eukaryotes. They provide mechanical stability in stereocilia, microvilli, filopodia, stress fibers and the sperm acrosome. Bundles are typically stabilized by a wide range of specific crosslinking proteins, most of which exhibit off-rates on the order of 1s−1. Yet F-actin bundles exhibit structural and mechanical integrity on time scales that are orders of magnitude longer. By applying large deformations to reconstituted F-actin bundles using optical tweezers, we provide direct evidence of their differential mechanical response in vitro: bundles exhibit fully reversible, elastic response on short time scales and irreversible, elasto-plastic response on time scales that are long compared to the characteristic crosslink dissociation time. Our measurements show a broad range of characteristic relaxation times for reconstituted F-actin bundles. This can be reconciled by considering that bundle relaxation behavior is also modulated by the number of filaments, crosslinking type and occupation number as well as the consideration of defects due to filament ends.

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
Fig. 7
Fig. 8

References

  • Aragon SR, Pecora R (1985) Dynamics of wormlike chains. Macromolecules 18(10):1868–1875. doi:10.1021/ma00152a014

    Article  CAS  Google Scholar 

  • Aratyn YS, Schaus TE, Taylor EW, Borisy GG (2007) Intrinsic dynamic behavior of fascin in filopodia. Mol Biol Cell 18(10):3928–3940. doi:10.1091/mbc.E07-04-0346

    Article  CAS  PubMed  Google Scholar 

  • Bartles JR (2000) Parallel actin bundles and their multiple actin-bundling proteins. Curr Opin Cell Biol 12(1):72–78. doi:10.1016/S0955-0674(99)00059-9

    Article  CAS  PubMed  Google Scholar 

  • Bathe M, Heussinger C, Claessens MM, Bausch AR, Frey E (2008) Cytoskeletal bundle mechanics. Biophys J 94(8):2955–2964. doi:10.1529/biophysj.107.119743

    Article  CAS  PubMed  Google Scholar 

  • Claessens MMAE, Bathe M, Frey E, Bausch AR (2006) Actin-binding proteins sensitively mediate F-actin bundle stiffness. Nat Mat 5(9):748–753. doi:10.1038/nmat1718

    Article  CAS  Google Scholar 

  • Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Fredberg JJ (2001) Scaling the microrheology of living cells. Phys Rev Lett 87(14):148–102. doi:10.1103/PhysRevLett.87.148102

    Article  CAS  Google Scholar 

  • Fazli H, Golestanian R (2007) Aggregation kinetics of stiff polyelectrolytes in the presence of multivalent salt. Phys Rev E 76(4):041–801.doi:10.1103/PhysRevE.76.041801

    Article  Google Scholar 

  • Fernandez P, Pullarkat PA, Ott A (2006) A master relation defines the nonlinear viscoelasticity of single fibroblasts. Biophys J 90(10):3796–3805. doi:10.1529/biophysj.105.072215

    Article  CAS  PubMed  Google Scholar 

  • Ferrer JM, Lee H, Chen J, Pelz B, Nakamura F, Kamm RD, Lang MJ (2008) Measuring molecular rupture forces between single actin filaments and actin-binding proteins. Proc Natl Acad Sci USA 105(27):9221–9226. doi:10.1073/pnas.0706124105

    Article  CAS  PubMed  Google Scholar 

  • Heintzelman MB, Mooseker MS (1992) Assembly of the intestinal brush border cytoskeleton. Curr Top Dev Biol 26:93–122

    Article  CAS  PubMed  Google Scholar 

  • Heussinger C, Schaefer B, Frey E (2007) Nonaffine rubber elasticity for stiff polymer networks. Phys Rev E Stat Nonlin Soft Matter Phys 76(3 Pt 1):031,906

    Google Scholar 

  • Hoffman BD, Massiera G, Citters KMV, Crocker JC (2006) The consensus mechanics of cultured mammalian cells. Proc Natl Acad Sci 103(27):10259–10264. doi:10.1073/pnas.0510348103

    Article  CAS  Google Scholar 

  • Hosek M, Tang JX (2004) Polymer-induced bundling of f actin and the depletion force. Phys Rev E 69(5):051,907. doi:10.1103/PhysRevE.69.051907

  • Hotulainen P, Lappalainen P (2006) Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 173(3):383–394. doi:10.1083/jcb.200511093

    Article  CAS  PubMed  Google Scholar 

  • Howard J (2001) Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • Janmey PA, Hvidt S, Käs J, Lerche D, Maggs A, Sackmann E, Schliwa M, Stossel TP (1994) The mechanical properties of actin gels. elastic modulus and filament motions. J Biol Chem 269(51):32503–32513

    CAS  Google Scholar 

  • Käs J, Strey H, Tang JX, Finger D, Ezzell R, Sackmann E, Janmey PA (1996) F-actin, a model polymer for semiflexible chains in dilute, semidilute, and liquid crystalline solutions. Biophys J 70(2)

  • Katoh K, Kano Y, Masuda M, Onishi H, Fujiwara K (1998) Isolation and contraction of the stress fiber. Mol Biol Cell 9(7):1919–1938

    CAS  PubMed  Google Scholar 

  • Koch D, Betz T, Ehrlicher A, Gogler M, Stuhrmann B, Käs J, Dholakia K, Spalding GC (2004) Optical control of neuronal growth. In: Optical Trapping and Optical Micromanipulation, SPIE, Denver, CO, USA, vol 5514, pp 428–436

  • Koenderink GH, Dogic Z, Nakamura F, Bendix PM, MacKintosh FC, Hartwig JH, Stossel TP, Weitz DA (2009) An active biopolymer network controlled by molecular motors. Proc Natl Acad Sci 106(36):15192–15197. doi:10.1073/pnas.0903974106

    Article  CAS  Google Scholar 

  • Kumar S, Maxwell IZ, Heisterkamp A, Polte TR, Lele TP, Salanga M, Mazur E, Ingber DE (2006) Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys J 90(10):3762–3773. doi:10.1529/biophysj.105.071506

    Article  CAS  PubMed  Google Scholar 

  • Lai GH, Coridan R, Zribi OV, Golestanian R, Wong GCL (2007) Evolution of growth modes for polyelectrolyte bundles. Phys Rev Lett 98(18):187,802. doi:10.1103/PhysRevLett.98.187802

    Article  Google Scholar 

  • Meeusen RL, Cande WZ (1979) N-ethylmaleimide-modified heavy meromyosin. a probe for actomyosin interactions. J Cell Biol 82(1):57–65

    Article  CAS  PubMed  Google Scholar 

  • Pollard T, Earnshaw W (2002) Cell biology. Elsevier Science, Philadelphia

    Google Scholar 

  • Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302(5651):1704–1709. doi:10.1126/science.1092053

    Article  CAS  PubMed  Google Scholar 

  • Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Ann Rev Cell Biol 4:63–92. doi:10.1146/annurev.cb.04.110188.000431

    CAS  PubMed  Google Scholar 

  • Semmrich C, Storz T, Glaser J, Merkel R, Bausch AR, Kroy K (2007) Glass transition and rheological redundancy in f-actin solutions. Proc Natl Acad Sci 104(51):20199–20203. doi:10.1073/pnas.0705513104

    Article  CAS  Google Scholar 

  • Sheetz M, Chasan R, Spudich J (1984) ATP-dependent movement of myosin in vitro: characterization of a quantitative assay. J Cell Biol 99(5):1867–1871

    Article  CAS  PubMed  Google Scholar 

  • Shin JH, Mahadevan L, So P, Matsudaira P (2004) Bending stiffness of a crystalline actin bundle. J Mol Biol 337(2):255–261. doi:10.1016/j.jmb.2004.01.028

    Article  CAS  PubMed  Google Scholar 

  • Smith D, Ziebert F, Humphrey D, Duggan C, Steinbeck M, Zimmermann W, Käs J (2007) Molecular motor-induced instabilities and cross linkers determine biopolymer organization. Biophys J 93(12):4445–4452. doi:10.1529/biophysj.106.095919

    Article  CAS  Google Scholar 

  • Stuhrmann B, Jahnke H, Schmidt M, Jähn K, Betz T, Müller K, Rothermel A, Käs J, Robitzki AA (2006) Versatile optical manipulation system for inspection, laser processing, and isolation of individual living cells. Rev Sci Instrum 77(6):063116-1–063116-11. doi:10.1063/1.2214961

    Article  Google Scholar 

  • Taute KM, Pampaloni F, Frey E, Florin E (2008) Microtubule dynamics depart from the wormlike chain model. Phys Rev Lett 100(2):028102-1–028102-4. doi:10.1103/PhysRevLett.100.028102

    Article  Google Scholar 

  • Tolomeo JA, Holley MC (1997) Mechanics of microtubule bundles in pillar cells from the inner ear. Biophys J 73(4):2241–2247

    Article  CAS  PubMed  Google Scholar 

  • Trepat X, Lenormand G, Fredberg JJ (2008) Universality in cell mechanics. Soft Matter 4(9):1750–1759

    Article  CAS  Google Scholar 

  • Wachsstock D, Schwartz W, Pollard T (1993) Affinity of alpha-actinin for actin determines the structure and mechanical properties of actin filament gels. Biophys J 65(1):205–214. doi:10.1016/S0006-3495(93)81059-2

    Article  CAS  PubMed  Google Scholar 

  • Wottawah F, Schinkinger S, Lincoln B, Ananthakrishnan R, Romeyke M, Guck J, Käs J (2005) Optical rheology of biological cells. Phys Rev Lett 94(9):098–103. doi:10.1103/PhysRevLett.94.098103

    Google Scholar 

  • Xu J, Wirtz D, Pollard TD (1998) Dynamic cross-linking by alpha-Actinin determines the mechanical properties of actin filament networks. J Biol Chem 273(16):9570–9576. doi:10.1074/jbc.273.16.9570

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Florian Huber, Jens Glaser and Klaus Kroy for helpful discussions. This work was supported by Leipzig School of Natural Sciences, “Building with Molecules and Nano-Objects” (BuildMoNa), and by DFG Graduiertenkolleg “InterNeuro” (GRK 1097) in Leipzig. M.B. is supported by MIT faculty start-up funds and the Samuel A. Goldblith Career Development Professorship. C.H. was supported by the Humboldt Foundation in the form of a Feodor Lynen research fellowship.

Author information

Author notes

  1. José Alvarado & Brian Gentry

    Present address: Biological Soft Matter Group, FOM Institute AMOLF, Science Park 104, 1098 XG, Amsterdam, The Netherlands

Authors and Affiliations

  1. Soft matter physics division, Institute for Experimental Physics I, University of Leipzig, 04103, Leipzig, Germany

    Dan Strehle, Jörg Schnauß, José Alvarado, Josef Käs & Brian Gentry

  2. Laboratoire de Physique de la Matière Condensée et Nanostructures, UMR CNRS 5586, Université de Lyon I, 69622, Villeurbanne, France

    Claus Heussinger

  3. Department of Biological Engineering, MIT, 77 Massachusetts Avenue, Cambridge, MA, 02139, USA

    Mark Bathe

Authors
  1. Dan Strehle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jörg Schnauß
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claus Heussinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José Alvarado
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mark Bathe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Josef Käs
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Brian Gentry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dan Strehle.

Electronic supplementary material

Below is the link to the electronic supplementary material.

PDF (317 KB)

PDF (556 KB)

PDF (288 KB)

PDF (1080 KB)

PDF (630 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Strehle, D., Schnauß, J., Heussinger, C. et al. Transiently crosslinked F-actin bundles. Eur Biophys J 40, 93–101 (2011). https://doi.org/10.1007/s00249-010-0621-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-010-0621-z

Keywords

Search

Navigation