Journal of Materials Science

, Volume 42, Issue 21, pp 8771–8787 | Cite as

Superelasticity, energy dissipation and strain hardening of vimentin coiled-coil intermediate filaments: atomistic and continuum studies

Nano- and micromechanical properties of hierarchical biological materials


Vimentin coiled-coil alpha-helical dimers are elementary protein building blocks of intermediate filaments, an important component of the cell’s cytoskeleton that has been shown to control the large-deformation behavior of eukaryotic cells. Here we use a combination of atomistic simulation and continuum theory to model tensile and bending deformation of single alpha-helices as well as coiled-coil double helices of the 2B segment of the vimentin dimer. We find that vimentin dimers can be extended to tensile strains up to 100% at forces below 50 pN, until strain hardening sets in with rapidly rising forces, approaching 8 nN at 200% strain. We systematically explore the differences between single alpha-helical structures and coiled-coil superhelical structures. Based on atomistic simulation, we discover a transition in deformation mechanism under varying pulling rates, resulting in different strength criteria for the unfolding force. Based on an extension of Bell’s theory that describes the dependence of the mechanical unfolding force on the pulling rate, we develop a fully atomistically informed continuum model of the mechanical properties of vimentin coiled-coils that is capable of predicting its nanomechanical behavior over a wide range of deformation rates that include experimental conditions. This model enables us to describe the mechanics of cyclic stretching experiments, suggesting a hysteresis in the force–strain response, leading to energy dissipation as the protein undergoes repeated tensile loading. We find that the dissipated energy increases continuously with increasing pulling rate. Our atomistic and continuum results help to interpret experimental studies that have provided evidence for the significnificance of vimentin intermediate filaments for the large-deformation regime of eukaryotic cells. We conclude that vimentin dimers are superelastic, highly dissipative protein assemblies.


  1. 1.
    Alberts B et al (2002) In: Molecular biology of the cell. Taylor & FrancisGoogle Scholar
  2. 2.
    Strelkov SV, Herrmann H, Aebi U (2003) BioEssays 25:243CrossRefGoogle Scholar
  3. 3.
    Burkhard P, Kammerer RA, Steinmetz MO, Bourenkov GP, Aebi U (2000) Structure 8:223CrossRefGoogle Scholar
  4. 4.
    Herrmann H, Aebi U (2004) Annu Rev Biochem 73:749CrossRefGoogle Scholar
  5. 5.
    Strelkov SV, Herrmann H, Geisler N, Wedig T, Zimbelmann R, Aebi U, Burkhard P (2002) EMBO J 6:1255CrossRefGoogle Scholar
  6. 6.
    Kiss B, Karsai A, Kellermayer MSZ (2006) J Struct Biol 155:327CrossRefGoogle Scholar
  7. 7.
    Janmey PA, Euteneuer U, Traub P, Schliwa M (1991) J Cell Biol 113:155CrossRefGoogle Scholar
  8. 8.
    Mücke N, Wedig T, Bürer A, Marekov L, Steinert P, Langowski J, Aebi U, Herrmann H (2004) J Mol Biol 340:97CrossRefGoogle Scholar
  9. 9.
    Smith TA, Strelkov SV, Burkhard P, Aebi U, Parry DAD (2002) J Struct Biol 137:128CrossRefGoogle Scholar
  10. 10.
    Wilson KL, Zastrow MS, Lee KK (2001) Cell 104:647Google Scholar
  11. 11.
    Wang N, Stamenovic D (2003) J Muscle Res Cell Motil 23:535CrossRefGoogle Scholar
  12. 12.
    Mücke N, Kreplak L, Kirmse R, Wedig T, Herrmann H, Aebi U, Langowski J (2004) J Mol Biol 355:2342Google Scholar
  13. 13.
    Helfand BT, Chang L, Goldman RD (2004) J Cell Sci 117:133CrossRefGoogle Scholar
  14. 14.
    Smith TA, Hempstead PD, Palliser CC, Parry DAD (2003) Proteins 50:207CrossRefGoogle Scholar
  15. 15.
    Kreplak L, Aebi U, Herrmann H (2004) Exp Cell Res 301:77CrossRefGoogle Scholar
  16. 16.
    Strelkov SV, Schumacher J, Burkhard P, Aebi U, Herrmann H (2004) J Mol Biol 343:1067CrossRefGoogle Scholar
  17. 17.
    Moir RD, Spann TP (2001). Cell Mol Life Sci 58:1748CrossRefGoogle Scholar
  18. 18.
    Coulombe PA, Bousquet O, Ma L, Yamada S, Wirtz D (2000) Cell Biol 10:420Google Scholar
  19. 19.
    Fudge DS, Gosline JM (2004) Proc R Soc Lond 271:291CrossRefGoogle Scholar
  20. 20.
    Fudge DS, Gardner KH, Forsyth VT, Riekel C Gosline JM (2003) Biophys J 85:2015Google Scholar
  21. 21.
    Eckes B, Dogic D, Colucci-Guyon E, Wang N., Maniotis A, Ingber D (1998) J Cell Sci 111:1897Google Scholar
  22. 22.
    Brown MJ, Hallam JA, Colucci-Guyon E, Shaw S (2001) J Immunol 166:6640Google Scholar
  23. 23.
    Nieminen M, Henttinen T, Merinen M, Marttila- Ichihara F, Eriksson JE, Jalkanen S (2006) Nat Cell Biol 8:156CrossRefGoogle Scholar
  24. 24.
    Kreplak L, Bär H, Leterrier JF, Herrmann H, Aebi U (2005) J Mol Biol 354:569Google Scholar
  25. 25.
    Storm C., Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA (2005) Nature 435:191CrossRefGoogle Scholar
  26. 26.
    Guzmán C, Jeney S, Kreplak L, Kasas S, Kulik AJ, Aebi U, Forró L (2006) J Mol Biol 360:623CrossRefGoogle Scholar
  27. 27.
    Omary MB, Coulombe PA, Irwin McLean WH (2004) N Engl J Med 351:2087CrossRefGoogle Scholar
  28. 28.
    Schietke R, Broehl D, Wedig T, Muecke N, Herrmann H, Magin TM (2006) Eur J Cell Biol 85:1CrossRefGoogle Scholar
  29. 29.
    Schwaiger I, Sattler C, Hostetter D, Rief M (2002) Nat Mater 1:232CrossRefGoogle Scholar
  30. 30.
    Akkermans RL, Warren CPB (2004) Phil Trans R Soc Lond 362:1783CrossRefGoogle Scholar
  31. 31.
    Root DD, Yadavalli VK, Forbes JF, Wang K (2006) Biophys J 90:2852CrossRefGoogle Scholar
  32. 32.
    Cieplak M, Hoang TX, Robbins MO (2002) Proteins: Struct Funct Genet 49:104CrossRefGoogle Scholar
  33. 33.
    Rohs R, Etchebest C, Lavery R (1999) Biophys J 76:2760Google Scholar
  34. 34.
    Bornschloegl T, Rief M (2006) PRL 96:118102CrossRefGoogle Scholar
  35. 35.
    Mitsui J, Nakajima K, Arakawa H, Hara M, Ikai A (2000) Biochem Biophys Res Commun 272:55CrossRefGoogle Scholar
  36. 36.
    Hanke F, Kreuzer HJ (2006) Phys Rev 74:031909Google Scholar
  37. 37.
    Evan E, Ritchie K (1997) Biophys J 72:1541Google Scholar
  38. 38.
    Dudko OK, Hummer G, Szabo A (2006) PRL 96:108101CrossRefGoogle Scholar
  39. 39.
    Wiita AP, Ainavarapu SRK, Huang HH, Fernandez JM (2006) PNAS 103:7222CrossRefGoogle Scholar
  40. 40.
    Gilli P, Bertolasi V, Pretto L, Gilli G (2006) J Mol Struct 790:40CrossRefGoogle Scholar
  41. 41.
    Bell GI (1978) Science 200:618CrossRefGoogle Scholar
  42. 42.
    Lu H, Isralewitz B, Krammer A, Vogel V, Schulten K (1998) Biophys J 75:662CrossRefGoogle Scholar
  43. 43.
    MacKerell AD et al (1998) J Phys Chem 102:3586Google Scholar
  44. 44.
    Courtney TH (1990) In: Mechanical behaviour of materials. McGraw-HillGoogle Scholar
  45. 45.
    Humphrey W, Dalke A, Schulten K (1996) J Mol Graphs 14:33CrossRefGoogle Scholar
  46. 46.
    Sheu SY, Yang DY, Selzle HL, Schlag EW (2003) PNAS 100:12683CrossRefGoogle Scholar
  47. 47.
    Inoué S, Salmon ED (1995) Mol Biol Cell 6(12):1619Google Scholar
  48. 48.
    Papadopoulos P et al (2006) Biomacromolecules 7:618CrossRefGoogle Scholar
  49. 49.
    Buehler MJ, Wand SY (in press) Entropic elasticity controls nanomechanics of single tropocollagen molecules Google Scholar
  50. 50.
    Buehler MJ (2007) J Mech Mater Struct (in print)Google Scholar
  51. 51.
    Baker D (2000) Nature 405:39CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental EngineeringMassachusetts Institute of TechnologyCambridgeUSA

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