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Self-Organized Nuclear Positioning Synchronizes the Cell Cycle in Drosophila Embryos.

Publication ,  Journal Article
Deneke, VE; Puliafito, A; Krueger, D; Narla, AV; De Simone, A; Primo, L; Vergassola, M; De Renzis, S; Di Talia, S
Published in: Cell
May 2, 2019

The synchronous cleavage divisions of early embryogenesis require coordination of the cell-cycle oscillator, the dynamics of the cytoskeleton, and the cytoplasm. Yet, it remains unclear how spatially restricted biochemical signals are integrated with physical properties of the embryo to generate collective dynamics. Here, we show that synchronization of the cell cycle in Drosophila embryos requires accurate nuclear positioning, which is regulated by the cell-cycle oscillator through cortical contractility and cytoplasmic flows. We demonstrate that biochemical oscillations are initiated by local Cdk1 inactivation and spread through the activity of phosphatase PP1 to generate cortical myosin II gradients. These gradients cause cortical and cytoplasmic flows that control proper nuclear positioning. Perturbations of PP1 activity and optogenetic manipulations of cortical actomyosin disrupt nuclear spreading, resulting in loss of cell-cycle synchrony. We conclude that mitotic synchrony is established by a self-organized mechanism that integrates the cell-cycle oscillator and embryo mechanics.

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Published In

Cell

DOI

EISSN

1097-4172

Publication Date

May 2, 2019

Volume

177

Issue

4

Start / End Page

925 / 941.e17

Location

United States

Related Subject Headings

  • Phosphoric Monoester Hydrolases
  • Myosin Type II
  • Mitosis
  • Microtubules
  • Embryonic Development
  • Embryo, Nonmammalian
  • Drosophila melanogaster
  • Drosophila Proteins
  • Developmental Biology
  • Cytoskeleton
 

Citation

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Deneke, V. E., Puliafito, A., Krueger, D., Narla, A. V., De Simone, A., Primo, L., … Di Talia, S. (2019). Self-Organized Nuclear Positioning Synchronizes the Cell Cycle in Drosophila Embryos. Cell, 177(4), 925-941.e17. https://doi.org/10.1016/j.cell.2019.03.007
Deneke, Victoria E., Alberto Puliafito, Daniel Krueger, Avaneesh V. Narla, Alessandro De Simone, Luca Primo, Massimo Vergassola, Stefano De Renzis, and Stefano Di Talia. “Self-Organized Nuclear Positioning Synchronizes the Cell Cycle in Drosophila Embryos.Cell 177, no. 4 (May 2, 2019): 925-941.e17. https://doi.org/10.1016/j.cell.2019.03.007.
Deneke VE, Puliafito A, Krueger D, Narla AV, De Simone A, Primo L, et al. Self-Organized Nuclear Positioning Synchronizes the Cell Cycle in Drosophila Embryos. Cell. 2019 May 2;177(4):925-941.e17.
Deneke, Victoria E., et al. “Self-Organized Nuclear Positioning Synchronizes the Cell Cycle in Drosophila Embryos.Cell, vol. 177, no. 4, May 2019, pp. 925-941.e17. Pubmed, doi:10.1016/j.cell.2019.03.007.
Deneke VE, Puliafito A, Krueger D, Narla AV, De Simone A, Primo L, Vergassola M, De Renzis S, Di Talia S. Self-Organized Nuclear Positioning Synchronizes the Cell Cycle in Drosophila Embryos. Cell. 2019 May 2;177(4):925-941.e17.
Journal cover image

Published In

Cell

DOI

EISSN

1097-4172

Publication Date

May 2, 2019

Volume

177

Issue

4

Start / End Page

925 / 941.e17

Location

United States

Related Subject Headings

  • Phosphoric Monoester Hydrolases
  • Myosin Type II
  • Mitosis
  • Microtubules
  • Embryonic Development
  • Embryo, Nonmammalian
  • Drosophila melanogaster
  • Drosophila Proteins
  • Developmental Biology
  • Cytoskeleton