Skip to main content
NCBI home page
Journal of Biological Physics logoLink to Journal of Biological Physics
. 2005 Dec;31(3-4):487–500. doi: 10.1007/s10867-005-7288-1

Nonlinear Dynamics of Microtubules: Biophysical Implications

M V Sataric 1, J A Tuszynski 2,✉
PMCID: PMC3456346  PMID: 23345913

Abstract

A recently developed model of nonlinear dynamics for microtubules is further expanded based on the biophysical arguments involving the secondary structure of the constitutive protein tubulin and on the ferroelectric properties of microtubules. It is demonstrated that kink excitations arise due to GTP hydrolysis that causes a dynamical transition in the structure of tubulin. The presence of an intrinsic electric field associated with the structure of a microtubule leads to unidirectional propagation of the kink excitation along the microtubule axis. This mechanism offers an explanation of the dynamic instability phenomenon in terms of the electric field effects. Moreover, a possible elucidation of the unidirectional transport of cargo via motor proteins such as kinesin and dynein is proposed within the model developed in this paper.

Key words: microtubule, tubulin, ferroelectricity, kink propagation, GTP hydrolysis, dynamic instability

Full Text

The Full Text of this article is available as a PDF (734.1 KB).

References

  1. Gross S.P.Hither and Yon: A Review of Bi-Directional Microtubule-Based Transport Phys. Biol. 20041R1–R11. 10.1088/1478-3967/1/2/R012004PhLA..331....1G [DOI] [PubMed] [Google Scholar]
  2. Alberts B., Bray A., Lewis D., Ratt M. J., Roberts K., Watson J.D. Molecular Biology of the Cell. New York: Garland Press; 2000. [Google Scholar]
  3. Mitchison T.J., Kirchner M.V.Dynamic Instability of Microtubule Growth Nature 1984312232–235.1984Natur.312..232M [DOI] [PubMed] [Google Scholar]
  4. Tulub, A.A.: Mg2+ Cofactor in a Triplet State Reduces a Proton pf a Coordinated Water Molecule to the Hydrogen Atom and Pushes it out of the Complex at a High Speed, Biofizika (Russian) 47 (2002), 20–26. [PubMed]
  5. Hol W.G. The Role of the α-Helix Dipole in Protein Function and Structure. Prog. Biophys. Mol. Biol. 1985;45:149–195. doi: 10.1016/0079-6107(85)90001-x. [DOI] [PubMed] [Google Scholar]
  6. Athenstaedt H.Pyroelectric and piezoelectric properties of vertebrates Ann. NY Acad. Sci. 197423868–93.1974NYASA.238...68A [DOI] [PubMed] [Google Scholar]
  7. Weitzel E.K., Tasker R., Brownell W.E.Outer Hair Cell Piezoelectricity; Frequency Response Enhancement and Resonance Behavior J. Acoust. Soc. Am. 20031141462–1466.2003ASAJ..114.1462W [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Tuszynski, J.A., Carpenter, E.J., Crawford, E., Brown, J.A., Malinski, W. and Dixon, J.M.: Molecular dynamics calculations of the electrostatic properties of tubulin and their consequences for microtubules, in W. Badawy and W. Moussa (eds.) Proceedings of ICMENS 2003, International Conference on MEMS, NANO and Smart Systems, Banff, IEEE Computer Society, Los Alamitos, CA, 2003, pp. 56–61.
  9. Baker N., Sept D., Joseph S., Holst M.J., McCammon J.A.Electrostatics of Nanosystems: Application to Microtubules the Ribosome Proc. Natl. Acad. Sci. U.S.A 20019810037–10041. 10.1073/pnas.1813423982001PNAS...9810037B [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Sataric M.V., Tuszynski J.A., Zakula R.B.Kinklike Excitations as an Energy-Transfer Mechanism in Microtubules Phys. Rev. E 199348589–597.1993PhRvE..48..589S [DOI] [PubMed] [Google Scholar]
  11. Zaccai G.How Soft is a Protein? A Protein Dynamic Force Constant Measured by Neutron Scattering Science 20002881604–1607. 10.1126/science.288.5471.16042000Sci...288.1604Z [DOI] [PubMed] [Google Scholar]
  12. Vale R.D., Milligan R.A.The Way Things Move; Looking Under the Hood of Molecular Motor Proteins Science 200022888–95.2000Sci...288...88V [DOI] [PubMed] [Google Scholar]
  13. Uyeda T.Q.P., Abramson P.D., Spudich J.A.The Neck Region of the Myosin Motor Domain Acts as a Lever Arm to Generate Movement Proc. Nat. Acad. Sci. U.S.A 1996934459–4464.1996PNAS...93.4459U [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Sataric, M.V. and Tuszynski, J.A.: The Relationship Between the Nonlinear Ferroelectric and Liquid Crystal Models for Microtubules, Phys. Rev. E67 (2003), 011901-1–011901-11. [DOI] [PubMed]
  15. Chretien D., Flyvbjerg H., Fuller S. Limited Flexibility of the Inter-Protofilament Bonds in Microtubules Assembled from Pure Tubulin. Eur. Biophys. J. 1998;27:490–500. doi: 10.1007/s002490050159. [DOI] [PubMed] [Google Scholar]
  16. Trpisova B., Tuszynski J.A.A Possible Link Between GTP Hydrolysis and Solitary Waves in Microtubules Phys. Rev. E 1997553288–3302.1997PhRvE..55.3288T [Google Scholar]
  17. Mejillano M.R., Barton J.S., Himes R.H. Stabilization of Microtubules by GTP Analogues. Biochem. Biophys. Res. Commun. 1990;166:653–660. doi: 10.1016/0006-291X(90)90859-L. [DOI] [PubMed] [Google Scholar]
  18. O'Brien E. T., Salmon E.D., Erickson H.P. How Calcium Causes Microtubule Depolymerization. Cell Motil. Cytoskeleton. 1997;36:125–135. doi: 10.1002/(SICI)1097-0169(1997)36:2<125::AID-CM3>3.0.CO;2-8. [DOI] [PubMed] [Google Scholar]
  19. Dhamodharm R., Jordan M.A., Thrower D., Wilson L., Wadsworth P. Vinblastine Suppresses Dynamics of Individual Microtubules in Living Interphase Cells. Mol. Biol. Cell. 1995;6:1215–1229. doi: 10.1091/mbc.6.9.1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sataric M.V., Zekovic S., Tuszynski J.A., Pokorny J.The Mössbauer Effect as a Possible Tool in Detecting Nonlinear Excitations in Microtubules Phys. Rev. E 1998586333–6339.1998PhRvE..58.6333S 10.1103/PhysRevE.58.6333 [DOI] [Google Scholar]

Articles from Journal of Biological Physics are provided here courtesy of Springer Science+Business Media B.V.

RESOURCES