Oscillatory movements of monooriented chromosomes and their position relative to the spindle pole result from the ejection properties of the aster and half-spindle
- PMID: 3733881
- PMCID: PMC2113830
- 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
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.
Similar articles
-
Micromanipulation of chromosomes in mitotic vertebrate tissue cells: tension controls the state of kinetochore movement.Exp Cell Res. 1997 Sep 15;235(2):314-24. doi: 10.1006/excr.1997.3691. Exp Cell Res. 1997. PMID: 9299155
-
Microtubule assembly and kinetochore directional instability in vertebrate monopolar spindles: implications for the mechanism of chromosome congression.J Cell Sci. 1994 Jan;107 ( Pt 1):285-97. doi: 10.1242/jcs.107.1.285. J Cell Sci. 1994. PMID: 8175915
-
The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores.J Cell Biol. 1995 Aug;130(4):941-8. doi: 10.1083/jcb.130.4.941. J Cell Biol. 1995. PMID: 7642709 Free PMC article.
-
Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle.J Cell Biol. 1994 Feb;124(3):223-33. doi: 10.1083/jcb.124.3.223. J Cell Biol. 1994. PMID: 8294508 Free PMC article. Review.
-
Biomechanics of chromosome alignment at the spindle midplane.Curr Biol. 2021 May 24;31(10):R574-R585. doi: 10.1016/j.cub.2021.03.082. Curr Biol. 2021. PMID: 34033791 Review.
Cited by
-
Mitosis - The story : Conly Rieder of the Wadsworth Center, Albany, NY, interviewed at the University of Exeter, UK, by James Wakefield and Herbert Macgregor, October 2010.Chromosome Res. 2011 Apr;19(3):275-90. doi: 10.1007/s10577-010-9174-3. Chromosome Res. 2011. PMID: 21213038 No abstract available.
-
Kinesin-5 mediated chromosome congression in insect spindles.Cell Mol Bioeng. 2018 Feb;11(1):25-36. doi: 10.1007/s12195-017-0500-0. Epub 2017 Aug 21. Cell Mol Bioeng. 2018. PMID: 29552234 Free PMC article.
-
Aberrantly segregating centromeres activate the spindle assembly checkpoint in budding yeast.J Cell Biol. 1996 Apr;133(1):75-84. doi: 10.1083/jcb.133.1.75. J Cell Biol. 1996. PMID: 8601615 Free PMC article.
-
Dynein prevents erroneous kinetochore-microtubule attachments in mitosis.Cell Cycle. 2015;14(21):3356-61. doi: 10.1080/15384101.2015.1089369. Cell Cycle. 2015. PMID: 26397382 Free PMC article.
-
Elevated polar ejection forces stabilize kinetochore-microtubule attachments.J Cell Biol. 2013 Jan 21;200(2):203-18. doi: 10.1083/jcb.201211119. J Cell Biol. 2013. PMID: 23337118 Free PMC article.