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. 1986 Aug 1;103(2):581–591. doi: 10.1083/jcb.103.2.581

Oscillatory movements of monooriented chromosomes and their position relative to the spindle pole result from the ejection properties of the aster and half-spindle

PMCID: PMC2113830  PMID: 3733881

Abstract

During mitosis a monooriented chromosome oscillates toward and away from its associated spindle pole and may be positioned many micrometers from the pole at the time of anaphase. We tested the hypothesis of Pickett-Heaps et al. (Pickett-Heaps, J. D., D. H. Tippit, and K. R. Porter, 1982, Cell, 29:729-744) that this behavior is generated by the sister kinetochores of a chromosome interacting with, and moving in opposite direction along, the same set of polar microtubules. When the sister chromatids of a monooriented chromosome split at the onset of anaphase in newt lung cells, the proximal chromatid remains stationary or moves closer to the pole, with the kinetochore leading. During this time the distal chromatid moves a variable distance radially away from the pole, with one or both chromatid arms leading. Subsequent electron microscopy of these cells revealed that the kinetochore on the distal chromatid is free of microtubules. These results suggest that the distal kinetochore is not involved in the positioning of a monooriented chromosome relative to the spindle pole or in its oscillatory movements. To test this conclusion we used laser microsurgery to create monooriented chromosomes containing one kinetochore. Correlative light and electron microscopy revealed that chromosomes containing one kinetochore continue to undergo normal oscillations. Additional observations on normal and laser-irradiated monooriented chromosomes indicated that the chromosome does not change shape, and that the kinetochore region is not deformed, during movement away from the pole. Thus movement away from the pole during an oscillation does not appear to arise from a push generated by the single pole-facing kinetochore fiber, as postulated (Bajer, A. S., 1982, J. Cell Biol., 93:33-48). When the chromatid arms of a monooriented chromosome are cut free of the kinetochore, they are immediately ejected radially outward from the spindle pole at a constant velocity of 2 micron/min. This ejection velocity is similar to that of the outward movement of an oscillating chromosome. We conclude that the oscillations of a monooriented chromosome and its position relative to the spindle pole result from an imbalance between poleward pulling forces acting at the proximal kinetochore and an ejection force acting along the chromosome, which is generated within the aster and half-spindle.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbott A. G., Hess J. E., Gerbi S. A. Spermatogenesis in Sciara coprophila. I. Chromosome orientation on the monopolar spindle of meiosis I. Chromosoma. 1981;83(1):1–18. doi: 10.1007/BF00286012. [DOI] [PubMed] [Google Scholar]
  2. Bajer A. S., Cypher C., Molè-Bajer J., Howard H. M. Taxol-induced anaphase reversal: evidence that elongating microtubules can exert a pushing force in living cells. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6569–6573. doi: 10.1073/pnas.79.21.6569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bajer A. S. Functional autonomy of monopolar spindle and evidence for oscillatory movement in mitosis. J Cell Biol. 1982 Apr;93(1):33–48. doi: 10.1083/jcb.93.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Hays T. S., Wise D., Salmon E. D. Traction force on a kinetochore at metaphase acts as a linear function of kinetochore fiber length. J Cell Biol. 1982 May;93(2):374–389. doi: 10.1083/jcb.93.2.374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hill T. L. Microfilament or microtubule assembly or disassembly against a force. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5613–5617. doi: 10.1073/pnas.78.9.5613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kubai D. F. Meiosis in Sciara coprophila: structure of the spindle and chromosome behavior during the first meiotic division. J Cell Biol. 1982 Jun;93(3):655–669. doi: 10.1083/jcb.93.3.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Mazia D., Paweletz N., Sluder G., Finze E. M. Cooperation of kinetochores and pole in the establishment of monopolar mitotic apparatus. Proc Natl Acad Sci U S A. 1981 Jan;78(1):377–381. doi: 10.1073/pnas.78.1.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. McIntosh J. R., Euteneuer U. Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J Cell Biol. 1984 Feb;98(2):525–533. doi: 10.1083/jcb.98.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. McNeill P. A., Berns M. W. Chromosome behavior after laser microirradiation of a single kinetochore in mitotic PtK2 cells. J Cell Biol. 1981 Mar;88(3):543–553. doi: 10.1083/jcb.88.3.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mitchison T., Kirschner M. Dynamic instability of microtubule growth. Nature. 1984 Nov 15;312(5991):237–242. doi: 10.1038/312237a0. [DOI] [PubMed] [Google Scholar]
  11. Nicklas R. B. Measurements of the force produced by the mitotic spindle in anaphase. J Cell Biol. 1983 Aug;97(2):542–548. doi: 10.1083/jcb.97.2.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. OSTERGREN G., MOLE-BAJER J., BAJER A. An interpretation of transport phenomena at mitosis. Ann N Y Acad Sci. 1960 Oct 7;90:381–408. doi: 10.1111/j.1749-6632.1960.tb23258.x. [DOI] [PubMed] [Google Scholar]
  13. Pickett-Heaps J. D., Tippit D. H., Porter K. R. Rethinking mitosis. Cell. 1982 Jul;29(3):729–744. doi: 10.1016/0092-8674(82)90435-4. [DOI] [PubMed] [Google Scholar]
  14. Rieder C. L., Bajer A. S. Effect of elevated temperatures on spindle microtubules and chromosome movements in cultured newt lung cells. Cytobios. 1978;18(71-72):201–233. [PubMed] [Google Scholar]
  15. Rieder C. L. Ribonucleoprotein staining of centrioles and kinetochores in newt lung cell spindles. J Cell Biol. 1979 Jan;80(1):1–9. doi: 10.1083/jcb.80.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rieder C. L. The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int Rev Cytol. 1982;79:1–58. doi: 10.1016/s0074-7696(08)61672-1. [DOI] [PubMed] [Google Scholar]
  17. Roos U. P. Light and electron microscopy of rat kangaroo cells in mitosis. I. Formation and breakdown of the mitotic apparatus. Chromosoma. 1973;40(1):43–82. doi: 10.1007/BF00319836. [DOI] [PubMed] [Google Scholar]
  18. Salmon E. D., Leslie R. J., Saxton W. M., Karow M. L., McIntosh J. R. Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching. J Cell Biol. 1984 Dec;99(6):2165–2174. doi: 10.1083/jcb.99.6.2165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Scholey J. M., Porter M. E., Grissom P. M., McIntosh J. R. Identification of kinesin in sea urchin eggs, and evidence for its localization in the mitotic spindle. Nature. 1985 Dec 5;318(6045):483–486. doi: 10.1038/318483a0. [DOI] [PubMed] [Google Scholar]
  20. Schulze E., Kirschner M. Microtubule dynamics in interphase cells. J Cell Biol. 1986 Mar;102(3):1020–1031. doi: 10.1083/jcb.102.3.1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Seto T., Kezer J., Pomerat C. M. A cinematographic study of meiosis in salamander spermatocytes in vitro. Z Zellforsch Mikrosk Anat. 1969;94(3):407–424. doi: 10.1007/BF00319185. [DOI] [PubMed] [Google Scholar]
  22. Vale R. D., Schnapp B. J., Mitchison T., Steuer E., Reese T. S., Sheetz M. P. Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. Cell. 1985 Dec;43(3 Pt 2):623–632. doi: 10.1016/0092-8674(85)90234-x. [DOI] [PubMed] [Google Scholar]

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