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Spatial structures in microtubular solutions requiring a sustained energy source

Abstract

MICROTUBULES are believed to be the principal organizers of the cell interior1. Cells respond to a variety of stimuli by modifying the spatial distribution of the microtubules. These effects are central to cell division and morphogenesis2, and embryo development3. During embryo development, macroscopic patterns are frequently observed3. Here we report that microtubular solutions spontaneously form alternating white and dark stripes about 1 mm wide and 1 cm long. Small-angle neutron scattering measurements show that in each segment the microtubules are aligned obliquely to the direction of the stripe, and that the white and dark stripes differ in having mutually orthogonal orientations. The formation of these structures requires an initial reservoir of organic phosphate. Phosphorus NMR measurements show that the process is accompanied by the energy-liberating conversion of organic to inorganic phosphate. These observations, together with similarities to the dissipative spatial structure formed by the Belousov–Zhabotinski reaction4–6, provide strong evidence that the observed structures are energy-dissipative in nature. Dissipative structures are thought to be critical to the appearence of complex living organisms7,8. Our results strongly suggest that microtubules are capable of forming such structures. Microtubular dissipative structures may occur during mitosis and embryo morphogenesis.

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References

  1. Alberts, B. et al. Molecular Biology of the Cell (Garland, New York, 1983).

    Google Scholar 

  2. Kirschner, M. & Mitchison, T. Cell 45, 329–342 (1986).

    Article  CAS  Google Scholar 

  3. Davidson, E. H. Gene Activity in Early Development (Academic, London, 1986).

    Google Scholar 

  4. Tyson, J. J. The Belousov-Zhabotinski Reaction, Lecture Notes in Biophysics (Springer, Berlin, 1976).

    Book  Google Scholar 

  5. Field, R. J. & Burger, M. (eds) Oscillations and Travelling Waves in Chemical Systems (Wiley, New York, 1985).

  6. Glansdorff, P. & Prigogine, I. Thermodynamic Theory of Structure, Stability and Fluctuations (Wiley-lnterscience, New York, 1971).

    MATH  Google Scholar 

  7. Nicolis, G. & Prigogine, I. Self Organisation in Nonequilibrium Systems (Wiley-lntersciences, New York, 1977).

    MATH  Google Scholar 

  8. Prigogine, I. & Stengers, I. Order Out of Chaos (Heinemann, London, 1984).

    Google Scholar 

  9. Job, D., Pabion, M. & Margolis, R. J. Cell. Biol. 101, 1680–1689 (1985).

    Article  CAS  Google Scholar 

  10. Jacrot, B. Rep. Prog. Phys. 39, 911–953 (1976).

    Article  ADS  CAS  Google Scholar 

  11. Bordas, J., Mandelkow, E. M. & Mandelkow, E. J. molec. Biol. 164, 89–135 (1983).

    Article  CAS  Google Scholar 

  12. Federov, B. et al. FEBS Lett. 84, 153–155 (1977).

    Article  Google Scholar 

  13. Onsager, L. Ann. N.Y. Acad. Sci. 51, 627–659 (1949).

    Article  ADS  CAS  Google Scholar 

  14. Haken, H. Synergetics (Springer. Berlin, 1978).

    Book  Google Scholar 

  15. Vidal, Ch. La Recherche 20, 1476–1485 (1989).

    CAS  Google Scholar 

  16. Bergé, P., Pomean, Y. & Vidal, Ch. Order Within Chaos (Wiley, New York. 1987).

    Google Scholar 

  17. Murray, J. D. Mathematical Biology (Springer, Berlin, 1989).

    Book  Google Scholar 

  18. Turing, A. M. Phil. Trans. R. Soc. B237, 37–72 (1952).

    Article  Google Scholar 

  19. de Gennes, P. G. The Physics of Liquid Crystals (Clarendon, Oxford, 1974).

    MATH  Google Scholar 

  20. Miike, H., Ochiai, K., Hashimoto, H. & Ebina, Y. J. phys. Soc. Jap. 54, 1724–1729 (1985).

    Article  ADS  CAS  Google Scholar 

  21. Pirollet, F., Job, D., Margolis, R. & Garel, J. R. EMBO J. 6, 3247–3252 (1987).

    Article  CAS  Google Scholar 

  22. Carlier, M. F., Melki, R., Pantaloni, D., Hill, T. L. & Chen, Y. Proc. natn. Acad. Sci. U.S.A. 84, 5257–5262 (1987)

    Article  ADS  CAS  Google Scholar 

  23. Mandelkow, E. M., Lange, G., Jagla, A., Spann, U. & Mandelkow, E. EMBO J. 7, 357–365 (1988).

    Article  CAS  Google Scholar 

  24. Dustin, P. Microtubules (Springer, Berlin, 1984).

    Book  Google Scholar 

  25. Carlier, M. F. & Pantaloni, D. Biochemistry 20, 1918–1924 (1981).

    Article  CAS  Google Scholar 

  26. Wilson, L., Snyder, K. B., Thompson, W. C. & Margolis, R. L. Meth. Cell Biol. A24, 159–169 (1982).

    Article  CAS  Google Scholar 

  27. Lonberg, F., Fraden, S., Hurd, A. & Meyer, R. Phys. Rev. Lett. 52, 1903–1906 (1984).

    Article  ADS  CAS  Google Scholar 

  28. Mandelkow, E., Mandelkow, E. M., Hotari, E. M., Hess, B. & Muller, S. Science 246, 1291–1293 (1989).

    Article  ADS  CAS  Google Scholar 

  29. Hitt, A., Cross, A. & Williams, R. J. biol. Chem. 265, 1639–1647 (1990).

    CAS  PubMed  Google Scholar 

  30. Rebhun, L. I. & Sander, G. J. Cell. Biol. 34, 859–884 (1967).

    Article  CAS  Google Scholar 

  31. Handbook of Neutron-beam Facilities Available for Users (Institut Laue-Langevin, Grenoble, 1981).

Download references

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Tabony, J., Job, D. Spatial structures in microtubular solutions requiring a sustained energy source. Nature 346, 448–451 (1990). https://doi.org/10.1038/346448a0

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