Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts

Abstract

Functional nuclei and mitotic spindles are shown to assemble around DNA-coated beads incubated in Xenopus egg extracts. Bipolar spindles assemble in the absence of centrosomes and kinetochores, indicating that bipolarity is an intrinsic property of microtubules assembling around chromatin in a mitotic cytoplasm. Microtubules nucleated at dispersed sites with random polarity rearrange into two arrays of uniform polarity. Spindle-pole formation requires cytoplasmic dynein-dependent translocation of microtubules across one another. It is proposed that spindles form in the absence of centrosomes by motor-dependent sorting of microtubules according to their polarity.

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References

  1. 1

    Telzer, B. R. & Haimo, L. T. J. Cell Biol. 89, 373–378 (1981).

  2. 2

    Mclntosh, J. R. & Euteneuer, U. J. Cell Biol. 98, 525–533 (1984).

  3. 3

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

  4. 4

    Inoue, S. & Salmon, E. D. Molec. cell. Biol. 6, 1619–1640 (1995).

  5. 5

    Hyman, A. A. & Karsenti, E. Cell 84, 401–411 (1996).

  6. 6

    Theurkauf, W. E. & Hawley, R. A. J. Cell Biol. 116, 1167–1180 (1992).

  7. 7

    Gard, D. L. Devl Biol. 151, 516–530 (1992).

  8. 8

    Lambert, A. M. & Lloyd, C. W. in Microtubules (eds Hyams, J. & Lloyd, C. W.) 325–342 (Wiley-Liss, New York, 1994).

  9. 9

    Bajer, A. S. & Mole Bajer, J. Cold Spring Harb. Symp. quant. Biol. 46, 263–283 (1982).

  10. 10

    Albertson, D. G. & Thomson, J. N. Chromosome Res. 1, 15–26 (1993).

  11. 11

    Karsenti, E., Newport, J. & Kirschner, M. J. Cell Biol. 99, 47s–57s (1984).

  12. 12

    Sawin, K. E. & Mitchison, T. J. J. Cell Biol. 112, 925–940 (1990).

  13. 13

    Zhang, D. & Nicklas, R. B. J. Cell Biol. 129, 1287–1300 (1995).

  14. 14

    Sandaltzopoulos, R., Blank, T. & Becker, P. B. EMBO J. 13, 373–379 (1994).

  15. 15

    Swanson, C. P., Merz, T. & Young, W. J. Cytogenetics 494–496 (Prentice Hall, Englewood Cliffs, 1981).

  16. 16

    Lourim, D. & Krohne, G. J. Cell Biol. 123, 501–512 (1993).

  17. 17

    Weis, K., Mattaj, I. W. & Lamond, A. I. Science 268, 1049–1053 (1995).

  18. 18

    Gard, D. L., Hafezi, S., Zhang, T. & Doxsey, S. J. J. Cell Biol. 110, 2033–2042 (1990).

  19. 19

    Vernos, I. & Karsenti, E. Curr. Opin. Cell Biol. 8, 4–9 (1996).

  20. 20

    Urrutia, R., McNiven, M. A., Albanesi, J. P., Murphy, D. B. & Kachar, B. Proc. natn. Acad. Sci. U.S.A. 88, 6701–6705 (1991).

  21. 21

    Hyman, A. A. J. Cell Sci. (suppl.) 14, 125–127 (1991).

  22. 22

    Vale, R. D., Reese, T. S. & Sheetz, M. P. Cell 42, 39–50 (1985).

  23. 23

    Shpetner, H. S., Paschal, B. M. & Vallee, R. B. J. Cell Biol. 107, 1001–1009 (1988).

  24. 24

    Steuer, E. R., Wordeman, L., Schroer, T. A. & Sheetz, M. P. Nature 345, 266–268 (1990).

  25. 25

    Dogterom, M., Felix, M.-A. & Guet, C. C. & Liebler, S. J. Cell Biol. 133, 125–140 (1996).

  26. 26

    Pellman, D., Bagget, M., Tu, H. & Fink, G. R. J. Cell Biol. 130, 1373–1385 (1995).

  27. 27

    Verde, F., Berrez, J. M., Antony, C. & Karsenti, E. J. Cell Biol. 112, 1177–1187 (1991).

  28. 28

    Vernos, I. & Karsenti, E. Trends Cell Biol. 5, 297–301 (1995).

  29. 29

    Pfarr, C. M. et al. Nature 345, 263–265 (1990).

  30. 30

    Echeverri, C. J., Paschal, B. M., Vaughan, K. T. & Vallee, R. B. J. Cell Biol. 132, 617–634 (1996).

  31. 31

    Murray, A. M. Meth. Cell Biol. 36, 591–603 (1991).

  32. 32

    Mitchison, T. J. a. K. & Kirschner, M. W. Nature 312, 232–236 (1984).

  33. 33

    Hyman, A. A. et al. Meth Enzym. 196, 478–485 (1991).

  34. 34

    Verde, F., Dogterom, M., Stelzer, E., Karsenti, E. & Leibler, S. J. Cell Biol. 118, 1097–1108 (1992).

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Heald, R., Tournebize, R., Blank, T. et al. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382, 420–425 (1996). https://doi.org/10.1038/382420a0

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