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Movement of chromosomes with severed kinetochore microtubules

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Abstract

Experiments dating from 1966 and thereafter showed that anaphase chromosomes continued to move poleward after their kinetochore microtubules were severed by ultraviolet microbeam irradiation. These observations were initially met with scepticism as they contradicted the prevailing view that kinetochore fibre microtubules pulled chromosomes to the pole. However, recent experiments using visible light laser microbeam irradiations have corroborated these earlier experiments as anaphase chromosomes again were shown to move poleward after their kinetochore microtubules were severed. Thus, multiple independent studies using different techniques have shown that chromosomes can indeed move poleward without direct microtubule connections to the pole, with only a kinetochore ‘stub’ of microtubules. An issue not yet settled is: what propels the disconnected chromosome? There are two not necessarily mutually exclusive proposals in the literature: (1) chromosome movement is propelled by the kinetochore stub interacting with non-kinetochore microtubules and (2) chromosome movement is propelled by a spindle matrix acting on the stub. In this review, we summarise the data indicating that chromosomes can move with severed kinetochore microtubules and we discuss proposed mechanisms for chromosome movement with severed kinetochore microtubules.

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Fig. 1

Notes

  1. 1.

    However, in Videos S1 and S4 of Sikirzhytski et al. (2014), illustrating severing of kinetochore microtubules in metaphase and anaphase, the associated chromosomes moved as described by Elting et al. (2014).

  2. 2.

    Crane-fly spermatocyte chromosomes do not change speed when kinetochore microtubules are severed; possible reasons [discussed in Forer et al. (2003)] may relate to the physical connections (‘tethers’) between separating half-bivalents and to signalling between half-bivalents.

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Acknowledgments

This study was supported by grants (to AF) from the Natural Sciences and Engineering Research Council of Canada and grant MCB0817107 (to KMJ) from the National Science Foundation.

Author information

Correspondence to Arthur Forer.

Additional information

Handling Editor: David Robinson

Electronic supplementary material

Below is the link to the electronic supplementary material.

Single images for the montage in Fig. 1 were taken from this sequence. The sequence begins in late metaphase. The upper left autosomal fibre was irradiated in early anaphase, from frame 19463 (time: 16:24:01) until frame 19477 (16:24:12), for a total of about 11 seconds. (MP4 13643 kb)

Supplementary Video 1

Single images for the montage in Fig. 1 were taken from this sequence. The sequence begins in late metaphase. The upper left autosomal fibre was irradiated in early anaphase, from frame 19463 (time: 16:24:01) until frame 19477 (16:24:12), for a total of about 11 seconds. (MP4 13643 kb)

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Forer, A., Johansen, K.M. & Johansen, J. Movement of chromosomes with severed kinetochore microtubules. Protoplasma 252, 775–781 (2015). https://doi.org/10.1007/s00709-014-0752-7

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Keywords

  • Spindle matrix
  • Ultraviolet microbeam irradiation
  • Laser microbeam irradiation