Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 Nov 1;109(5):2245–2255. doi: 10.1083/jcb.109.5.2245

The motor for poleward chromosome movement in anaphase is in or near the kinetochore

PMCID: PMC2115846  PMID: 2808528

Abstract

I have tested two contending views of chromosome-to-pole movement in anaphase. Chromosomes might be pulled poleward by a traction fiber consisting of the kinetochore microtubules and associated motors, or they might propel themselves by a motor in the kinetochore. I cut through the spindle of demembranated grasshopper spermatocytes between the chromosomes and one pole and swept the polar region away, removing a portion of the would-be traction fiber. Chromosome movement continued, and in the best examples, chromosomes moved to within 1 micron of the cut edge. There is nothing beyond the edge to support movement, and a push from the rear is unlikely because cuts in the interzone behind the separating chromosomes did not stop movement. Therefore, I conclude that the motor must be in the kinetochore or within 1 micron of it. Less conclusive evidence points to the kinetochore itself as the motor. The alternative is an external motor pulling on the kinetochore microtubules or directly on the kinetochore. A pulling motor would move kinetochore microtubules along with the chromosome, so that in a cut half-spindle, the microtubules should protrude from the cut edge as chromosomes move toward it. No protrusion was seen; however, the possibility that microtubules depolymerize as they are extruded, though unlikely, is not ruled out. What is certain is that the motor for poleward chromosome movement in anaphase must be in the kinetochore or very close to it.

Full Text

The Full Text of this article is available as a PDF (3.4 MB).

Selected References

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

  1. Aist J. R., Berns M. W. Mechanics of chromosome separation during mitosis in Fusarium (Fungi imperfecti): new evidence from ultrastructural and laser microbeam experiments. J Cell Biol. 1981 Nov;91(2 Pt 1):446–458. doi: 10.1083/jcb.91.2.446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bajer A. S. Interaction of microtubules and the mechanism of chromosome movement (zipper hypothesis). 1. General principle. Cytobios. 1973 Nov;8(31):139–160. [PubMed] [Google Scholar]
  3. Cande W. Z., McDonald K. L. In vitro reactivation of anaphase spindle elongation using isolated diatom spindles. Nature. 1985 Jul 11;316(6024):168–170. doi: 10.1038/316168a0. [DOI] [PubMed] [Google Scholar]
  4. Cande W. Z. Nucleotide requirements for anaphase chromosome movements in permeabilized mitotic cells: anaphase B but not anaphase A requires ATP. Cell. 1982 Jan;28(1):15–22. doi: 10.1016/0092-8674(82)90370-1. [DOI] [PubMed] [Google Scholar]
  5. Cassimeris L., Inoué S., Salmon E. D. Microtubule dynamics in the chromosomal spindle fiber: analysis by fluorescence and high-resolution polarization microscopy. Cell Motil Cytoskeleton. 1988;10(1-2):185–196. doi: 10.1002/cm.970100123. [DOI] [PubMed] [Google Scholar]
  6. Cohn S. A., Pickett-Heaps J. D. The effects of colchicine and dinitrophenol on the in vivo rates of anaphase A and B in the diatom Surirella. Eur J Cell Biol. 1988 Aug;46(3):523–530. [PubMed] [Google Scholar]
  7. Forer A. Characterization of the mitotic traction system, and evidence that birefringent spindle fibers neither produce nor transmit force for chromosome movement. Chromosoma. 1966;19(1):44–98. doi: 10.1007/BF00332793. [DOI] [PubMed] [Google Scholar]
  8. Forer A. Do anaphase chromosomes chew their way to the pole or are they pulled by actin? J Cell Sci. 1988 Dec;91(Pt 4):449–453. doi: 10.1242/jcs.91.4.449. [DOI] [PubMed] [Google Scholar]
  9. Fuge H., Bastmeyer M., Steffen W. A model for chromosome movement based on lateral interaction of spindle microtubules. J Theor Biol. 1985 Aug 7;115(3):391–399. doi: 10.1016/s0022-5193(85)80199-5. [DOI] [PubMed] [Google Scholar]
  10. Gorbsky G. J., Sammak P. J., Borisy G. G. Chromosomes move poleward in anaphase along stationary microtubules that coordinately disassemble from their kinetochore ends. J Cell Biol. 1987 Jan;104(1):9–18. doi: 10.1083/jcb.104.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gorbsky G. J., Sammak P. J., Borisy G. G. Microtubule dynamics and chromosome motion visualized in living anaphase cells. J Cell Biol. 1988 Apr;106(4):1185–1192. doi: 10.1083/jcb.106.4.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hill T. L. Theoretical problems related to the attachment of microtubules to kinetochores. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4404–4408. doi: 10.1073/pnas.82.13.4404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hiramoto Y., Nakano Y. Micromanipulation studies of the mitotic apparatus in sand dollar eggs. Cell Motil Cytoskeleton. 1988;10(1-2):172–184. doi: 10.1002/cm.970100122. [DOI] [PubMed] [Google Scholar]
  14. Koshland D. E., Mitchison T. J., Kirschner M. W. Polewards chromosome movement driven by microtubule depolymerization in vitro. Nature. 1988 Feb 11;331(6156):499–504. doi: 10.1038/331499a0. [DOI] [PubMed] [Google Scholar]
  15. Margolis R. L., Wilson L., Keifer B. I. Mitotic mechanism based on intrinsic microtubule behaviour. Nature. 1978 Mar 30;272(5652):450–452. doi: 10.1038/272450a0. [DOI] [PubMed] [Google Scholar]
  16. Margolis R. L., Wilson L. Microtubule treadmills--possible molecular machinery. Nature. 1981 Oct 29;293(5835):705–711. doi: 10.1038/293705a0. [DOI] [PubMed] [Google Scholar]
  17. McIntosh J. R. Spindle structure and the mechanisms of chromosome movement. Basic Life Sci. 1985;36:197–229. doi: 10.1007/978-1-4613-2127-9_14. [DOI] [PubMed] [Google Scholar]
  18. Mitchison T., Evans L., Schulze E., Kirschner M. Sites of microtubule assembly and disassembly in the mitotic spindle. Cell. 1986 May 23;45(4):515–527. doi: 10.1016/0092-8674(86)90283-7. [DOI] [PubMed] [Google Scholar]
  19. Nicklas R. B. Chromosome movement and spindle birefringence in locally heated cells: interaction versus local control. Chromosoma. 1979 Sep 1;74(1):1–37. doi: 10.1007/BF00344480. [DOI] [PubMed] [Google Scholar]
  20. Nicklas R. B., Kubai D. F., Hays T. S. Spindle microtubules and their mechanical associations after micromanipulation in anaphase. J Cell Biol. 1982 Oct;95(1):91–104. doi: 10.1083/jcb.95.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nicklas R. B. Mitosis. Adv Cell Biol. 1971;2:225–297. doi: 10.1007/978-1-4615-9588-5_5. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Spurck T. P., Pickett-Heaps J. D. On the mechanism of anaphase A: evidence that ATP is needed for microtubule disassembly and not generation of polewards force. J Cell Biol. 1987 Oct;105(4):1691–1705. doi: 10.1083/jcb.105.4.1691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Vale R. D., Schnapp B. J., Reese T. S., Sheetz M. P. Organelle, bead, and microtubule translocations promoted by soluble factors from the squid giant axon. Cell. 1985 Mar;40(3):559–569. doi: 10.1016/0092-8674(85)90204-1. [DOI] [PubMed] [Google Scholar]
  25. Vigers G. P., Coue M., McIntosh J. R. Fluorescent microtubules break up under illumination. J Cell Biol. 1988 Sep;107(3):1011–1024. doi: 10.1083/jcb.107.3.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wolniak S. M. The regulation of mitotic spindle function. Biochem Cell Biol. 1988 Jun;66(6):490–514. doi: 10.1139/o88-061. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES