Anomalous flexural behaviors of microtubules.

Apparent controversies exist on whether the persistence length of microtubules depends on its contour length. This issue is particularly challenging from a theoretical point of view due to the tubular structure and strongly anisotropic material property of microtubules. Here we adopt a higher order continuum orthotropic thin shell model to study the flexural behavior of microtubules. Our model overcomes some key limitations of a recent study based on a simplified anisotropic shell model and results in a closed-form solution for the contour-length-dependent persistence length of microtubules, with predictions in excellent agreement with experimental measurements. By studying the ratio between their contour and persistence lengths, we find that microtubules with length at ~1.5 μm show the lowest flexural rigidity, whereas those with length at ~15 μm show the highest flexural rigidity. This finding may provide an important theoretical basis for understanding the mechanical structure of mitotic spindles during cell division. Further analysis on the buckling of microtubules indicates that the critical buckling load becomes insensitive to the tube length for relatively short microtubules, in drastic contrast to the classical Euler buckling. These rich flexural behaviors of microtubules are of profound implication for many biological functions and biomimetic molecular devices.

[1]  Akif Uzman,et al.  The cell cycle: Principles of control (Primers in Biology series) , 2007 .

[2]  F. MacKintosh,et al.  Deformation and collapse of microtubules on the nanometer scale. , 2003, Physical review letters.

[3]  C. Schönenberger,et al.  Nanomechanics of microtubules. , 2002, Physical review letters.

[4]  Chengyuan Wang,et al.  Axisymmetric and beamlike vibrations of multiwall carbon nanotubes , 2005 .

[5]  E. Nogales,et al.  High-Resolution Model of the Microtubule , 1999, Cell.

[6]  Yves Engelborghs,et al.  Dynamical and mechanical study of immobilized microtubules with atomic force microscopy , 1996 .

[7]  A C Maggs,et al.  Analysis of microtubule rigidity using hydrodynamic flow and thermal fluctuations. , 1994, The Journal of biological chemistry.

[8]  D. Chrétien,et al.  New data on the microtubule surface lattice , 1991, Biology of the cell.

[9]  H. Hess,et al.  Ratchet patterns sort molecular shuttles , 2002 .

[10]  B. Kirby Micro- and nanoscale fluid mechanics : transport in microfluidic devices , 2010 .

[11]  Manfred Schliwa,et al.  Molecular motors , 2003, Nature.

[12]  Tienchong Chang,et al.  Buckling of microtubules under bending and torsion , 2008 .

[13]  Donald E. Ingber,et al.  Jcb: Article Introduction , 2002 .

[14]  H Tashiro,et al.  Buckling of a single microtubule by optical trapping forces: direct measurement of microtubule rigidity. , 1995, Cell motility and the cytoskeleton.

[15]  R. Cross,et al.  Mechanics of the kinesin step , 2005, Nature.

[16]  D. Roos,et al.  Microtubules, but not actin filaments, drive daughter cell budding and cell division in Toxoplasma gondii. , 2000, Journal of cell science.

[17]  Nathan A. Baker,et al.  The physical basis of microtubule structure and stability , 2003, Protein science : a publication of the Protein Society.

[18]  A. Mioduchowski,et al.  Vibration of microtubules as orthotropic elastic shells , 2006 .

[19]  Huajian Gao,et al.  Persistence Length of Microtubules Based on a Continuum Anisotropic Shell Model , 2010 .

[20]  Saulius Juodkazis,et al.  Flexural Rigidity of a Single Microtubule , 2002 .

[21]  Harvey F. Lodish,et al.  MOLECULAR.CELL.BIOLOGY 5TH.ED , 2003 .

[22]  Viola Vogel,et al.  A piconewton forcemeter assembled from microtubules and kinesins , 2002 .

[23]  H. Lodish Molecular Cell Biology , 1986 .

[24]  C. Waterman-Storer,et al.  Cell motility: can Rho GTPases and microtubules point the way? , 2001, Journal of cell science.

[25]  M. Schliwa,et al.  Flexural rigidity of microtubules measured with the use of optical tweezers. , 1996, Journal of cell science.

[26]  M. Holley,et al.  Mechanics of microtubule bundles in pillar cells from the inner ear. , 1997, Biophysical journal.

[27]  A Mioduchowski,et al.  Orthotropic elastic shell model for buckling of microtubules. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  D. Sept,et al.  Microtubule elasticity: connecting all-atom simulations with continuum mechanics. , 2009, Physical review letters.

[29]  C. Q. Ru,et al.  Wave propagation in orthotropic microtubules , 2007 .

[30]  J. Bernholc,et al.  Nanomechanics of carbon tubes: Instabilities beyond linear response. , 1996, Physical review letters.

[31]  Hideo Tashiro,et al.  Flexural rigidity of individual microtubules measured by a buckling force with optical traps. , 2006, Biophysical journal.

[32]  Stéphanie Portet,et al.  Anisotropic elastic properties of microtubules , 2005, The European physical journal. E, Soft matter.

[33]  Erwin Frey,et al.  Thermal fluctuations of grafted microtubules provide evidence of a length-dependent persistence length , 2005, Proceedings of the National Academy of Sciences.

[34]  E. Meyhöfer,et al.  Directional loading of the kinesin motor molecule as it buckles a microtubule. , 1996, Biophysical journal.

[35]  Takahiro Nitta,et al.  Dispersion in active transport by kinesin-powered molecular shuttles. , 2005, Nano letters.

[36]  J. McIntosh,et al.  A molecular-mechanical model of the microtubule. , 2005, Biophysical journal.

[37]  Huajian Gao,et al.  A generalized bead-rod model for Brownian dynamics simulations of wormlike chains under strong confinement. , 2005, The Journal of chemical physics.

[38]  S. Edwards,et al.  The Theory of Polymer Dynamics , 1986 .

[39]  Hanqing Jiang,et al.  Mechanics of Microtubule Buckling Supported by Cytoplasm , 2008 .

[40]  C. Q. Ru,et al.  Effective bending stiffness of carbon nanotubes , 2000 .

[41]  D. Boal Mechanics of the Cell: Membranes , 2012 .

[42]  J. Howard,et al.  Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape , 1993, The Journal of cell biology.

[43]  E. Ghavanloo,et al.  Prediction of bending stiffness and deformed shape of non-axially compressed microtubule by a semi-analytical approach , 2010, Journal of biological physics.

[44]  K. Ewert,et al.  Synchrotron X-ray diffraction study of microtubules buckling and bundling under osmotic stress: a probe of interprotofilament interactions. , 2004, Physical review letters.