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Self-centring activity of cytoplasm

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Abstract

Fish melanophore cells aggregate pigment granules at the centre or redisperse them throughout the cytoplasm. The granules move along radial microtubules by means of molecular motors1–3. Cytoplasmic fragments of melanophores organize a radial array of microtubules and aggregate pigment at its centre4–7. Here we report self-centring in microsurgically produced cytoplasmic fragments of black tetra melanophores. We observed rapid (10 min) formation of a radial microtubule array after stimulation of aggregation. Arrangement of microtubules in the fragments returned to random during pigment redispersion. Apparently, formation of the radial array does not depend on a pre-existing microtubule-organizing centre. The array did not form in granule-free fragments nor in fragments treated with inhibitors of the intracellular motor protein cytoplasmic dynein. We conclude that formation of the radial microtubule array is induced by directional motion of pigment granules along microtubules and present evidence that its position is defined by interaction of microtubules with the surface.

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References

  1. Schliwa, M. Mechanisms of intracellular organelle transport, in Cell and Muscle Motility (ed. Shay, J. W.) 5, 1–82 (Plenum, New York and London, 1984).

    Google Scholar 

  2. Obika, M. Cytophysiology of fish chromatophores. Zool. Sci. (Tokyo) 3, 1–11 (1986).

    CAS  Google Scholar 

  3. Haimo, L. H. & Thaler, C. D. Regulation of organelle transport: lessons from color change in fish. BioEssays 16, 727–732 (1994).

    Article  Google Scholar 

  4. Matthews, S. Observations on pigment migration within the fish melanophore. J. Exp. Zool. 58, 471–486 (1931).

    Article  Google Scholar 

  5. McNiven, M., Wang, M. & Porter, K. R. Microtubule polarity and the direction of pigment transport reverse simultaneously in surgically severed melanophore arms. Cell 37, 753–765 (1984).

    Article  CAS  Google Scholar 

  6. McNiven, M. & Porter, K. R. Microtubule polarity confers direction of pigment transport in chromatophores. J. Cell Biol. 103, 1547–1555 (1986).

    Article  CAS  Google Scholar 

  7. McNiven, M. & Porter, K. R. Organization of microtubules in centrosome-free cytoplasm. J. Cell Biol. 106, 1593–1605 (1988).

    Article  CAS  Google Scholar 

  8. Rodionov, V. I., Gyoeva, F. K. & Gelfand, V. I. Kinesin is responsible for centrifugal movement of pigment granules in melanophores. Proc. Natl Acad. Sci. USA 88, 4956–4960 (1991).

    Article  ADS  CAS  Google Scholar 

  9. Oakley, B. γ-Tubulin. In: Microtubules (eds Hyams, J. S. and Lloid, C. W.) 33–45 (Wiley-Liss, New York, 1994).

    Google Scholar 

  10. Doxsey, S. J., Stein, P., Evans, L., Calarco, P. & Kirschner, M. Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76, 639–650 (1994).

    Article  CAS  Google Scholar 

  11. Paschal, B. M. & Vallee, R. B. Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330, 181–183 (1987).

    Article  ADS  CAS  Google Scholar 

  12. Shpetner, H. S., Paschal, B. M. & Vallee, R. B. Characterization of microtubule-activated ATPase of brain cytoplasmic dynein (MAP 1C). J. Cell Biol. 107, 1001–1009.

  13. Beckerle, M. C. & Porter, K. R. Inhibitors of dynein activity block intracellular transport in erythrophores. Nature 295, 701–703 (1982).

    Article  ADS  CAS  Google Scholar 

  14. Clark, T. G. & Rosenbaum, J. L. Pigment particle translocation in detergent-permeabilized melanophores of Fundulus heteroclitus. Proc. Natl. Acad. Sci. USA 79, 4655–4659 (1982).

    Article  ADS  CAS  Google Scholar 

  15. Vale, R. D., Reese, T. S. & Sheetz, M. P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39–50 (1985).

    Article  CAS  Google Scholar 

  16. Verde, F., Berrez, J.-M., Antony, C. & Karsenti, E. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112, 1177–1187 (1991).

    Article  CAS  Google Scholar 

  17. Heald, R., Tournebize, R., Blank, T., Sandaltzopoulos, R., Becker, P., Hyman, A. & Karsenti, E. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382, 420–425 (1996).

    Article  ADS  CAS  Google Scholar 

  18. Urrutia, R., McNiven, M., Albanesi, J. P., Murphy, D. B. & Kachar, B. Purified kinesin promotes vesicle motility and induces active sliding between microtubules in vitro. Proc. Natl. Acad. Sci. USA 88, 6701–6705 (1991).

    Article  ADS  CAS  Google Scholar 

  19. Gyoeva, F. K., Leonova, E. V., Rodionov, V. I. & Gelfand, V. I. Intermediate filaments in fish melanophores. J. Cell Sci. 88, 649–655 (1987).

    PubMed  Google Scholar 

  20. Rodionov, V. I., Lim, S.-S., Gelfand, V. I. & Borisy, G. G. Microtubule dynamics in melanophores. J. Cell Biol. 126, 1455–1464 (1994).

    Article  CAS  Google Scholar 

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Rodionov, V., Borisy, G. Self-centring activity of cytoplasm. Nature 386, 170–173 (1997). https://doi.org/10.1038/386170a0

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  • DOI: https://doi.org/10.1038/386170a0

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