Collision of Expanding Actin Caps with Actomyosin Borders for Cortical Bending and Mitotic Rounding in a Syncytium

• Published in: Developmental cell 2018-06, Vol.45 (5), p.551-564.e4
• Main Authors: Zhang, Yixie, Yu, Jessica C., Jiang, Tao, Fernandez-Gonzalez, Rodrigo, Harris, Tony J.C.
• Format: Article
• Language: English
• Subjects: actin; Actins - metabolism; Actomyosin - metabolism; Animals; Arp2/3; Cell Membrane; cortical domains; Drosophila; Drosophila melanogaster - genetics; Drosophila melanogaster - growth & development; Drosophila melanogaster - metabolism; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; embryo cleavage; Embryo, Nonmammalian - cytology; Embryo, Nonmammalian - metabolism; forces; Giant Cells - cytology; Giant Cells - physiology; mesoscale; Microtubules - metabolism; mitotic rounding; myosin; Spindle Apparatus - physiology; syncytium
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2018.04.024

The early Drosophila embryo is a large syncytial cell that compartmentalizes mitotic spindles with furrows. Before furrow ingression, an Arp2/3 actin cap forms above each nucleus and is encircled by actomyosin. We investigated how these networks transform a flat cortex into a honeycomb-like compartmental array. The growing caps circularize and ingress upon meeting their actomyosin borders, which become the furrow base. Genetic perturbations indicate that the caps physically displace their borders and, reciprocally, that the borders resist and circularize their caps. These interactions create an actomyosin cortex arrayed with circular caps. The Rac-GEF Sponge, Rac-GTP, Arp3, and actin coat the caps as a growing material that can drive cortical bending for initial furrow ingression. Additionally, laser ablations indicate that actomyosin contraction squeezes the cytoplasm, producing counterforces that swell the caps. Thus, Arp2/3 caps form clearances of the actomyosin cortex and control buckling and swelling of these clearances for metaphase compartmentalization. [Display omitted] •An embryo-wide actomyosin network becomes embedded with circular Arp2/3 domains•The Arp2/3 actin caps engage their actomyosin borders for mitotic rounding•Each growing actin cap collides with its border and buckles to form furrows•Contraction of the embryo-wide myosin network generates forces that swell the caps For mitosis in the syncytial Drosophila embryo, each nucleus organizes a surface Arp2/3 actin cap encircled by an actomyosin border. Zhang et al. show that the assembling caps and borders engage each other physically to pattern the syncytial cortex in 2D and to generate compartments for mitotic spindles in 3D.