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Nuclear repulsion enables division autonomy in a single cytoplasm.

Publication ,  Journal Article
Anderson, CA; Eser, U; Korndorf, T; Borsuk, ME; Skotheim, JM; Gladfelter, AS
Published in: Curr Biol
October 21, 2013

BACKGROUND: Current models of cell-cycle control, based on classic studies of fused cells, predict that nuclei in a shared cytoplasm respond to the same CDK activities to undergo synchronous cycling. However, synchrony is rarely observed in naturally occurring syncytia, such as the multinucleate fungus Ashbya gossypii. In this system, nuclei divide asynchronously, raising the question of how nuclear timing differences are maintained despite sharing a common milieu. RESULTS: We observe that neighboring nuclei are highly variable in division-cycle duration and that neighbors repel one another to space apart and demarcate their own cytoplasmic territories. The size of these territories increases as a nucleus approaches mitosis and can influence cycling rates. This nonrandom nuclear spacing is regulated by microtubules and is required for nuclear asynchrony, as nuclei that transiently come in very close proximity will partially synchronize. Sister nuclei born of the same mitosis are generally not persistent neighbors over their lifetimes yet remarkably retain similar division cycle times. This indicates that nuclei carry a memory of their birth state that influences their division timing and supports that nuclei subdivide a common cytosol into functionally distinct yet mobile compartments. CONCLUSIONS: These findings support that nuclei use cytoplasmic microtubules to establish "cells within cells." Individual compartments appear to push against one another to compete for cytoplasmic territory and insulate the division cycle. This provides a mechanism by which syncytial nuclei can spatially organize cell-cycle signaling and suggests size control can act in a system without physical boundaries.

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Published In

Curr Biol

DOI

EISSN

1879-0445

Publication Date

October 21, 2013

Volume

23

Issue

20

Start / End Page

1999 / 2010

Location

England

Related Subject Headings

  • Time-Lapse Imaging
  • Microscopy
  • Green Fluorescent Proteins
  • Giant Cells
  • Eremothecium
  • Developmental Biology
  • Cytoplasm
  • Cell Nucleus Division
  • 52 Psychology
  • 32 Biomedical and clinical sciences
 

Citation

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Anderson, C. A., Eser, U., Korndorf, T., Borsuk, M. E., Skotheim, J. M., & Gladfelter, A. S. (2013). Nuclear repulsion enables division autonomy in a single cytoplasm. Curr Biol, 23(20), 1999–2010. https://doi.org/10.1016/j.cub.2013.07.076
Anderson, Cori A., Umut Eser, Therese Korndorf, Mark E. Borsuk, Jan M. Skotheim, and Amy S. Gladfelter. “Nuclear repulsion enables division autonomy in a single cytoplasm.Curr Biol 23, no. 20 (October 21, 2013): 1999–2010. https://doi.org/10.1016/j.cub.2013.07.076.
Anderson CA, Eser U, Korndorf T, Borsuk ME, Skotheim JM, Gladfelter AS. Nuclear repulsion enables division autonomy in a single cytoplasm. Curr Biol. 2013 Oct 21;23(20):1999–2010.
Anderson, Cori A., et al. “Nuclear repulsion enables division autonomy in a single cytoplasm.Curr Biol, vol. 23, no. 20, Oct. 2013, pp. 1999–2010. Pubmed, doi:10.1016/j.cub.2013.07.076.
Anderson CA, Eser U, Korndorf T, Borsuk ME, Skotheim JM, Gladfelter AS. Nuclear repulsion enables division autonomy in a single cytoplasm. Curr Biol. 2013 Oct 21;23(20):1999–2010.
Journal cover image

Published In

Curr Biol

DOI

EISSN

1879-0445

Publication Date

October 21, 2013

Volume

23

Issue

20

Start / End Page

1999 / 2010

Location

England

Related Subject Headings

  • Time-Lapse Imaging
  • Microscopy
  • Green Fluorescent Proteins
  • Giant Cells
  • Eremothecium
  • Developmental Biology
  • Cytoplasm
  • Cell Nucleus Division
  • 52 Psychology
  • 32 Biomedical and clinical sciences