A cytokinetic ring-driven cell rotation achieves Hertwig's rule in early development

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Teije C. Middelkoop - , Max Planck Institute of Molecular Cell Biology and Genetics, Czech Academy of Sciences (Author)
  • Jonas Neipel - , Max-Planck-Institute for the Physics of Complex Systems (Author)
  • Caitlin E. Cornell - , University of California at Berkeley (Author)
  • Ronald Naumann - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Lokesh G. Pimpale - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Frank Jülicher - , Max-Planck-Institute for the Physics of Complex Systems, TUD Dresden University of Technology (Author)
  • Stephan W. Grill - , Clusters of Excellence PoL: Physics of Life, Biotechnology Center, Max Planck Institute of Molecular Cell Biology and Genetics (Author)

Abstract

Hertwig's rule states that cells divide along their longest axis, usually driven by forces acting on the mitotic spindle. Here, we show that in contrast to this rule, microtubule-based pulling forces in early Caenorhabditis elegans embryos align the spindle with the short axis of the cell. We combine theory with experiments to reveal that in order to correct this misalignment, inward forces generated by the constricting cytokinetic ring rotate the entire cell until the spindle is aligned with the cell's long axis. Experiments with slightly compressed mouse zygotes indicate that this cytokinetic ring-driven mechanism of ensuring Hertwig's rule is general for cells capable of rotating inside a confining shell, a scenario that applies to early cell divisions of many systems.

Details

Original languageEnglish
Article numbere2318838121
Pages (from-to)e2318838121
JournalProceedings of the National Academy of Sciences of the United States of America
Volume121
Issue number25
Publication statusPublished - 18 Jun 2024
Peer-reviewedYes

External IDs

PubMed 38870057

Keywords

ASJC Scopus subject areas

Keywords

  • actomyosin, biophysics, cell biology, cytokinesis, development, Zygote/metabolism, Caenorhabditis elegans/embryology, Spindle Apparatus/metabolism, Embryonic Development/physiology, Rotation, Microtubules/metabolism, Animals, Models, Biological, Cytokinesis/physiology, Embryo, Nonmammalian/cytology, Mice