Abstract
Segregating genetic material along the longest axis of the cell ensures that there is a sufficient distance between daughter chromosomes at the point of cytokinesis. Monitoring the orientation of the mitotic spindle can be subjected to cell cycle controls. In the fission yeast Schizosaccharomyces pombe, the existence of such a cell-cycle checkpoint has been proposed to delay the metaphase to anaphase transition when spindle poles are not properly oriented with respect to the actomyosin ring1. Here we show, by using a fission yeast mutant compromised in its assembly of astral microtubules, that in the absence of astral microtubules short metaphase spindles are unable to orient themselves with respect to the long axis of the cell and are delayed in spindle elongation. This astral defect engages a spindle orientation checkpoint because deletion of the transcription factor Atf1, which is involved in maintaining this checkpoint, allows misaligned asterless metaphase spindles to elongate. We propose that astral microtubules are involved directly in monitoring orientation of the metaphase spindle and in controlling the timing of elongation in fission yeast.
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References
Gachet, Y., Tournier, S., Millar, J. B. & Hyams, J. S. Nature. 412, 352–355 (2001).
Hagan, I. M. & Hyams, J. S. Cell Motil. Cytoskeleton. 34, 69–75 (1996).
Ding, D. Q., Chikashige, Y., Haraguchi, T. & Hiraoka, Y. J. Cell Sci. 111, 701–712 (1998).
Sparks, C. A., Morphew, M. & McCollum, D. J. Cell Biol. 146, 779–790 (1999).
Decottignies, A. & Nurse, P. J. Cell Sci. 114, 2627–2640 (2001).
Takeda, T. et al. EMBO J. 14, 6193–6208 (1995).
Wilkinson, M. G. et al. Genes Dev. 10, 2289–2301 (1996).
White, J. & Strome, S. Cell. 84, 195–198 (1996).
Carminati, J. L. & Stearns, T. J. Cell Biol. 138, 629–641 (1997).
Kaltschmidt, J. A., Davidson, C. M., Brown, N. H. & Brand, A. H. Nature Cell Biol. 2, 7–12 (2000).
Moreno, S., Klar, A. & Nurse, P. Methods Enzymol. 194, 795–823 (1991).
Balasubramanian, M. K., McCollum, D. & Gould, K. L. Methods Enzymol. 283, 494–506 (1997).
Acknowledgements
We thank Y. Hiraoka, J. Millar, A. Decottignies and K. Gull for materials and reagents; G. Jedd for comments on the manuscript; and members of the fungal laboratories, especially V. Rajagopalan, V. Wachtler, N. Naqvi and K. Wong for discussions. Our research was supported by A*STAR Singapore and Temasek Life Sciences Laboratory.
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Supplementary information
Supplementary figure and table
Figure S1 Mia1+ gene from S. pombe has an overall sequence homology to the hypothetical protein NCU01413.1from N. crassa. (PDF 214 kb)
Supplementary table 1
Movie 1
A time-lapse sequence of spindle dynamics in α-tubulin-EGFP expressing wild type S. pombe. (MOV 900 kb)
Movie 2
A time-lapse sequence of spindle dynamics in α-tubulin-EGFP expressing mia1Δ S. pombe cell. (MOV 1291 kb)
Movie 3
A time-lapse sequence of spindle dynamics, visualized using a Sid2p-EGFP expressed in wild type S. pombe. (MOV 672 kb)
Movie 4
A time-lapse sequence of spindle dynamics, visualized using a Sid2p-EGFP expressed in mia1Δ cell. (MOV 1068 kb)
Movie 5
A time-lapse sequence of spindle dynamics in α-tubulin-EGFP-expressing mia1Δatf1Δ cell. (MOV 926 kb)
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Oliferenko, S., Balasubramanian, M. Astral microtubules monitor metaphase spindle alignment in fission yeast. Nat Cell Biol 4, 816–820 (2002). https://doi.org/10.1038/ncb861
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DOI: https://doi.org/10.1038/ncb861
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