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Modeling anterograde and retrograde transport of short mobile microtubules from the site of axonal branch formation

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Abstract

This theoretical research is motivated by a recent model of microtubule (MT) transport put forward by Baas and Mozgova (Cytoskeleton 69:416–425, 2012). According to their model, in an axon all plus-end-distal mobile MTs move anterogradely while all minus-end-distal mobile MTs move retrogradely. Retrograde MT transport thus represents a mechanism by which minus-end-distal MTs are removed from the axon. We suggested equations that implement Baas and Mozgova’s model. We employed these equations to simulate transport of short mobile MTs from a region (such as the site of axonal branch formation) where MT severing activity results in generation of a large number of short MTs of both orientations. We obtained the exact and approximate transient solutions of these equations utilizing the Laplace transform technique. We applied the obtained solutions to calculate the average rates of anterograde and retrograde transport of short MTs.

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References

  1. Baas, P.W., Mozgova, O.I.: A novel role for retrograde transport of microtubules in the axon. Cytoskeleton 69, 416–425 (2012)

    Article  Google Scholar 

  2. Wang, L., Brown, A.: Rapid movement of microtubules in axons. Curr. Biol. 12, 1496–1501 (2002)

    Article  Google Scholar 

  3. Baas, P., Karabay, A., Qiang, L.: Microtubules cut and run. Trends Cell Biol. 15, 518–524 (2005)

    Article  Google Scholar 

  4. Baas, P., Nadar, C., Myers, K.: Axonal transport of microtubules: the long and short of it. Traffic 7, 490–498 (2006)

    Article  Google Scholar 

  5. Goldstein, L.S.B., Yang, Z.H.: Microtubule-based transport systems in neurons: the roles of kinesins and dyneins. Ann. Rev. Neurosci. 23, 39–71 (2000)

    Article  Google Scholar 

  6. Lu, W., Fox, P., Lakonishok, M., Davidson, M.W., Gelfand, V.I.: Initial neurite outgrowth in Drosophila neurons is driven by kinesin-powered microtubule sliding. Curr. Biol. 23, 1018–1023 (2013)

    Article  Google Scholar 

  7. He, Y., Francis, F., Myers, K.A., Yu, W.Q., Black, M.M., Baas, P.W.: Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J. Cell Biol. 168, 697–703 (2005)

    Article  Google Scholar 

  8. Ahmad, F., He, Y., Myers, K., Hasaka, T., Francis, F., Black, M., Baas, P.: Effects of dynactin disruption and dynein depletion on axonal microtubules. Traffic 7, 524–537 (2006)

    Article  Google Scholar 

  9. Myers, K.A., Baas, P.W.: Microtubule–actin interactions during neuronal development. In: Gallo, G., Lanier, L.M. (eds.) Neurobiology of Actin. Advances in Neurobiology, vol. 5, pp. 73–96. Springer, New York (2011)

    Chapter  Google Scholar 

  10. Hasaka, T., Myers, K., Baas, P.: Role of actin filaments in the axonal transport of microtubules. J. Neurosci. 24, 11291–11301 (2004)

    Article  Google Scholar 

  11. Zheng, Y., Wildonger, J., Ye, B., Zhang, Y., Kita, A., Younger, S.H., Zimmerman, S., Jan, L.Y., Jan, Y.N.: Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol. 10, 1172–1180 (2008)

    Article  Google Scholar 

  12. Dent, E., Callaway, J., Szebenyi, G., Baas, P., Kalil, K.: Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J. Neurosci. 19, 8894–8908 (1999)

    Google Scholar 

  13. Yu, W., Liang Qiang, Solowska, J.M., Karabay, A., Korulu, S., Baas, P.W.: The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol. Biol. Cell 19, 1485–1498 (2008)

    Article  Google Scholar 

  14. Gibson, D.A., Ma, L.: Developmental regulation of axon branching in the vertebrate nervous system. Development 138, 183–195 (2011)

    Article  Google Scholar 

  15. Jung, P., Brown, A.: Modeling the slowing of neurofilament transport along the mouse sciatic nerve. Phys. Biol. 6, 046002 (2009)

    Article  Google Scholar 

  16. Li, Y., Jung, P., Brown, A.: Axonal transport of neurofilaments: a single population of intermittently moving polymers. J Neurosci. 32, 746–758 (2012)

    Article  Google Scholar 

  17. Myers, K.A., Baas, P.W.: Kinesin-5 regulates the growth of the axon by acting as a brake on its microtubule array. J. Cell Biol. 178, 1081–1091 (2007)

    Article  Google Scholar 

  18. King, S.J., Schroer, T.A.: Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2, 20–24 (2000)

    Article  Google Scholar 

  19. Toba, S., Watanabe, T.M., Yamaguchi-Okimoto, L., Toyoshima, Y.Y., Higuchi, H.: Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. Proc. Nat. Acad. Sci. U. S. A. 103, 5741–5745 (2006)

    Article  ADS  Google Scholar 

  20. Kuznetsov, A.V.: An exact solution describing slow axonal transport of cytoskeletal elements: effect of a finite half-life. Proc. R. Soc. A Math. Phys. Eng. Sci. 468, 3384–3397 (2012)

    Article  ADS  Google Scholar 

  21. Kuznetsov, A.V.: An exact solution of transient equations describing slow axonal transport. Comput. Methods Biomech Biomed. Eng. 16, 1232–1239 (2013)

    Google Scholar 

  22. Tytell, M., Brady, S., Lasek, R.: Axonal-transport of a subclass of tau-proteins—evidence for the regional differentiation of microtubules in neurons. Proc. Nat. Acad. Sci. U. S. A. 81, 1570–1574 (1984)

    Article  ADS  Google Scholar 

  23. Galbraith, J.A., Reese, T.S., Schlief, M.L., Gallant, P.E.: Slow transport of unpolymerized tubulin and polymerized neurofilament in the squid giant axon. Proc. Nat. Acad. Sci. U. S. A. 96, 11589–11594 (1999)

    Article  ADS  Google Scholar 

  24. Roll-Mecak, A., Mcnally, F.J.: Microtubule-severing enzymes. Curr. Opin. Cell Biol. 22, 96–103 (2010)

    Article  Google Scholar 

  25. Black, M., Lasek, R.: Slow components of axonal-transport: two cytoskeletal networks. J. Cell Biol. 86, 616–623 (1980)

    Article  Google Scholar 

  26. Oblinger, M., Brady, S., McQuarrie, I., Lasek, R.: Cytotypic differences in the protein-composition of the axonally transported cytoskeleton in mammalian neurons. J. Neurosci. 7, 453–462 (1987)

    Google Scholar 

  27. Kuznetsov, I.A., Kuznetsov, A.V.: Analytical comparison between Nixon-Logvinenko and Jung-Brown theories of slow neurofilament transport in axons. Math. Biosci. 245, 331–339 (2013)

    Article  Google Scholar 

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Acknowledgements

The authors are indebted to the anonymous reviewers for their constructive comments. AVK gratefully acknowledges support of the Alexander von Humboldt Foundation though the Humboldt Research Award.

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Kuznetsov, I.A., Kuznetsov, A.V. Modeling anterograde and retrograde transport of short mobile microtubules from the site of axonal branch formation. J Biol Phys 40, 41–53 (2014). https://doi.org/10.1007/s10867-013-9334-8

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  • DOI: https://doi.org/10.1007/s10867-013-9334-8

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