Rate-dependent response of axonal microtubules and tau proteins under shear forces

Rate-dependent response of axonal microtubules and tau proteins under shear forces

Luca Bellino, Giuseppe Florio, Alain Goriely, Giuseppe Puglisi

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Abstract. The brain tissue is a very complex biological material exhibiting viscoelastic-type properties at the macroscopic level, arising from a hierarchical multiscale structure. Thus, to describe such interesting features at the molecular level, we introduce a model mimicking the coupling of microtubules and tau proteins inside the neuronal axon and we study the rate-dependent response under different conditions of applied load, rate, and temperature.

Rate Effects, Brain Tissue, Microtubules, Tau Proteins

Published online 3/17/2022, 6 pages
Copyright © 2023 by the author(s)
Published under license by Materials Research Forum LLC., Millersville PA, USA

Citation: Luca Bellino, Giuseppe Florio, Alain Goriely, Giuseppe Puglisi, Rate-dependent response of axonal microtubules and tau proteins under shear forces, Materials Research Proceedings, Vol. 26, pp 65-70, 2023

DOI: https://doi.org/10.21741/9781644902431-11

The article was published as article 11 of the book Theoretical and Applied Mechanics

Content from this work may be used under the terms of the Creative Commons Attribution 3.0 license. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.

[1] S. B. Smith, D. F. Meaney, Axonal damage in traumatic brain injury, The neuroscientist, 6, 6, 483 – 495, (2000). https://doi.org/10.1177/107385840000600611
[2] M.D. Tang-Schomer, A. R. Patel, P. W. Baas, D. H. Smith, Mechanical breaking of microtubules in axons during stretch injury underlies delayed elasticity, microtubule disassembly and axon degeneration, The FASEB Journal, 24, 5, 1401 – 1410, (2010). https://doi.org/10.1096/fj.09-142844
[3] C. Ballatore, V. M. Y. Lee, J. Q. Trojanowski, Tau-mediated neurodegeneration in Alzheimer’s disease and related disorders, Nature rev. neuroscience, 8, 9, 663 – 672, (2007). https://doi.org/10.1038/nrn2194
[4] Ya. Shi, W. Zhang, Y. Yang, A. G. Murzin, B. Falcon, A. Kotecha, M. van Beers, A. Tarutani, F. Kametani, H. J. Garringer et al, Structure-based classification of tauopathies, Nature, 598, 7880, 359 – 363, (2021). https://doi.org/10.1038/s41586-021-03911-7
[5] T. Hawkins, M. Mirigian, M. S. Yasar, J. L. Ross, Mechanics of microtubules, Journal of Biomechanics, 43, 1, 23 – 30, (2010). https://doi.org/10.1016/j.jbiomech.2009.09.005
[6] H. Ouyang, E. Neuman, R. Shi, Contribution of cytoskeletal elements to the axonal mechanical properties, Journal of biological engineering, 7, 1, 1 – 8, (2013). https://doi.org/10.1186/1754-1611-7-21
[7] D. S. Eisenberg, M. R. Sawaya, Taming tangled tau, Nature, 547, 7662, 170–171, (2017). https://doi.org/10.1038/nature23094
[8] K. J. J. Rosenberg, L. Ross, H. E. Feinstein, S. C: Feinstein, J. Israelachvili, Complementary dimerization of microtubule-associated tau protein: implications for microtubule bundling and tau-mediated pathogenesis, PNAS, 105, 21, 7445 – 7450, (2008). https://doi.org/10.1073/pnas.0802036105
[9] R. De Rooij, K. E. Miller, E. Kuhl, Modeling molecular mechanism in the axon, Computational mechanics, 59, 3, 523 – 537, (2017). https://doi.org/10.1007/s00466-016-1359-y
[10] H. Van den Bedem, E. Kuhl, Tau-ism: the Yin and Yang of microtubules sliding, detachment and rupture, Biophysical Journal, 109, 11, 2215, (2015). https://doi.org/10.1016/j.bpj.2015.10.020
[11] E. Evans, K. Ritchie, Dynamic strength of molecular adhesion bonds, Biophysical Journal, 72, 4, 1541 – 1555, (1997). https://doi.org/10.1016/S0006-3495(97)78802-7
[12] T. Cohen, S. Givli, Dynamics of a discrete chain of bi-stable elements: a biomimetic shock absorbing mechanism, JMPS, 64, 426 – 439, (2014). https://doi.org/10.1016/j.jmps.2013.12.010
[13] Y. R. Efendiev, L. Truskinovsky, Thermalization of a driven bi-stable FPU chain, Continuum mechanics and thermodynamics, 22, 6, 679 – 698, (2010). https://doi.org/10.1007/s00161-010-0166-5
[14] S. Givli, K. Bhattacharya, A coarse-grained model of the myofibril: overall dynamics and the evolution of sarcomere non-uniformities, JMPS, 57, 2, 221 – 243, (2009). https://doi.org/10.1016/j.jmps.2008.10.013
[15] R. Raj, P. K. Purohit, Phase boundaries as agents of structural change in macromolecules, JMPS, 59, 10, 2044 – 2069, (2011). https://doi.org/10.1016/j.jmps.2011.07.003
[16] L. Bellino, G. Florio, G. Puglisi, The influence of device handles in single molecule experiments, Soft Matter, 15, 43, 8680 – 8690, (2019). https://doi.org/10.1039/C9SM01376H
[17] M. Benedito, S. Giordano, Isotensional and isometric force-extension response of chains with bistable units, PRE, 98, 5, 052146, (2018). https://doi.org/10.1103/PhysRevE.98.052146
[18] I. Benichou, S. Givli, the hidden ingenuity of titin structure, Applied Physics Letters, 99, 091904, (2011). https://doi.org/10.1063/1.3558901
[19] L. Bellino, G. Florio, S. Giordano, G. Puglisi, On the competition between interface energy and temperature in phase transition phenomena, Application of Engineering Science, 2, 100009, (2020). https://doi.org/10.1016/j.apples.2020.100009
[20] A. Cannizzo, L. Bellino, G. Florio, G. Puglisi, S. Giordano, Thermal control of nucleation and propagation transition stresses in discrete lattices with non-local interactions and non-convex energy, EPJ Plus, 137, 569, (2022). https://doi.org/10.1140/epjp/s13360-022-02790-9
[21] A. Cannizzo, G. Florio, G. Puglisi, S. Giordano, Temperature controlled decohesion regimes of an elastic chain adhering to a fixed substrate by softening and breakable bonds, Journal of Physics A, 54, 445001, (2021). https://doi.org/10.1088/1751-8121/ac2a07
[22] S. Di Stefano, G. Florio, G. Napoli, N. M. Pugno, G. Puglisi, On the role of elasticity in focal adhesion within the passive regime, International Journal of Nonlinear Mechanics, accepted, (2022). https://doi.org/10.1016/j.ijnonlinmec.2022.104157
[23] V. Fazio, D. De Tommasi, N. M. Pugno, G. Puglisi, Spider Silks Mechanics: Predicting Humidity and Temperature Effects. JMPS, in press, (2022). https://doi.org/10.1016/j.jmps.2022.104857
[24] L. Bellino, G. Florio, A. Goriely, G. Puglisi, Role of interlinker stiffness in melting and unfolding cooperativity and toughness of double stranded peptide chains, Preprint, (2022).
[25] H. Herrmann, U. Aebi, Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds, Annual review of biochemistry, 73, 1, 749 – 789, (2012). https://doi.org/10.1146/annurev.biochem.73.011303.073823
[26] R. De Rooji, K. E. Miller, E. Kuhl, Modeling molecular mechanism in the axon, computational mechanics, 59, 3, 523 – 537, (2017). https://doi.org/10.1007/s00466-016-1359-y
[27] H. B. Da Rocha, L. Truskinovsky, Rigidity-controlled crossover, from spinodal to critical failure, PRL, 124, 1, 015501, (2020). https://doi.org/10.1103/PhysRevLett.124.015501
[28] G. I. Bell, Models for the specific adhesion of cells to cells, Science, 200, 4342, 618 – 627, (1978). https://doi.org/10.1126/science.347575
[29] P. Hanggi, P. Talkner, M. Borkovec, Reaction-rate theory: fifty years after Kramers, Reviews of modern physics, 62, 2, 251, (1990). https://doi.org/10.1103/RevModPhys.62.251
[30] H. A. Kramers, Brownian motion in a field of force and the diffusion model of chemical reactions, Physica, 7, 4, 284 – 304, (1940). https://doi.org/10.1016/S0031-8914(40)90098-2
[31] L. Bellino, G. Florio, A. Goriely, G. Puglisi, Effects of rate and temperature on the mechanical response of microtubules and tau proteins, Preprint, (2022).
[32] I. Benichou, Y. Zhang, O. K. Dudko, S. Givli, The rate dependent response of a bistable chain at finite temperature, JMPS, 95, 44 – 63, (2016). https://doi.org/10.1016/j.jmps.2016.05.001
[33] H. Ahmadzadeh, D. H. Smith, V. B. Shenoy, Mechanical effects of dynamic binding between tau proteins on microtubules during axonal injury, Biophysical Journal, 106, 5, 1123 – 1133, (2015). https://doi.org/10.1016/j.bpj.2014.01.024
[34] R. De Rooij, E. Kuhl, Physical biology of axonal damage, Frontiers in cellular neuroscience, 12, 144, (2018). https://doi.org/10.3389/fncel.2018.00144