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

Author:

Middelkoop Teije C.12ORCID,Neipel Jonas3ORCID,Cornell Caitlin E.4,Naumann Ronald1ORCID,Pimpale Lokesh G.1ORCID,Jülicher Frank35ORCID,Grill Stephan W.15ORCID

Affiliation:

1. Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany

2. Laboratory of Developmental Mechanobiology, Division Biocev, Institute of Molecular Genetics of the Czech Academy of Sciences, 14220 Prague, Czech Republic

3. Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany

4. Department of Bioengineering, University of California, Berkeley, CA 94720

5. Cluster of Excellence Physics of Life, Technical University Dresden, 01062 Dresden, Germany

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.

Funder

Grantová Agentura České Republiky

EC | European Research Council

Publisher

Proceedings of the National Academy of Sciences

Reference74 articles.

1. O. Hertwig, Welchen Einfluss übt die Schwerkraft auf die Theilung der Zellen? (Verlag von Gustav Fischer, Jena, 1884).

2. Ueber den Werth der ersten Furchungszellen für die Organbildung des Embryo Experimentelle Studien am Frosch-und Tritonei

3. Uber die Anordnung der Zellen in jungsten Pflanzentheilen;Sachs J.;Arb. Bot. Inst. Wurzbg.,1878

4. E. B. Wilson, The Cell in Development and Heredity (The Macmillan Company, 1925), (May 24, 2023).

5. Influence of Cell Geometry on Division-Plane Positioning

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