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Biophys J. 2016 Oct 18;111(8):1773-1784. doi: 10.1016/j.bpj.2016.09.007.

The Mitotic Spindle in the One-Cell C. elegans Embryo Is Positioned with High Precision and Stability.

Author information

1
Institute of Genetics and Development of Rennes, Unité Mixte de Recherche 6290, Centre National de la Recherche Scientifique, CS 34317, Rennes, France; Institute of Genetics and Development of Rennes, University Rennes 1, Rennes, France; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany. Electronic address: jacques.pecreaux@univ-rennes1.fr.
2
Dresden University of Technology, Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
3
Institute of Genetics and Development of Rennes, Unité Mixte de Recherche 6290, Centre National de la Recherche Scientifique, CS 34317, Rennes, France; Institute of Genetics and Development of Rennes, University Rennes 1, Rennes, France.
4
Shriram Center of Bioengineering and Chemical Engineering, Stanford University, Stanford, California; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
5
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
6
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, Connecticut. Electronic address: jonathon.howard@yale.edu.

Abstract

Precise positioning of the mitotic spindle is important for specifying the plane of cell division, which in turn determines how the cytoplasmic contents of the mother cell are partitioned into the daughter cells, and how the daughters are positioned within the tissue. During metaphase in the early Caenorhabditis elegans embryo, the spindle is aligned and centered on the anterior-posterior axis by a microtubule-dependent machinery that exerts restoring forces when the spindle is displaced from the center. To investigate the accuracy and stability of centering, we tracked the position and orientation of the mitotic spindle during the first cell division with high temporal and spatial resolution. We found that the precision is remarkably high: the cell-to-cell variation in the transverse position of the center of the spindle during metaphase, as measured by the standard deviation, was only 1.5% of the length of the short axis of the cell. Spindle position is also very stable: the standard deviation of the fluctuations in transverse spindle position during metaphase was only 0.5% of the short axis of the cell. Assuming that stability is limited by fluctuations in the number of independent motor elements such as microtubules or dyneins underlying the centering machinery, we infer that the number is ∼1000, consistent with the several thousand of astral microtubules in these cells. Astral microtubules grow out from the two spindle poles, make contact with the cell cortex, and then shrink back shortly thereafter. The high stability of centering can be accounted for quantitatively if, while making contact with the cortex, the astral microtubules buckle as they exert compressive, pushing forces. We thus propose that the large number of microtubules in the asters provides a highly precise mechanism for positioning the spindle during metaphase while assembly is completed before the onset of anaphase.

PMID:
27760363
PMCID:
PMC5071606
DOI:
10.1016/j.bpj.2016.09.007
[Indexed for MEDLINE]
Free PMC Article

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