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

Abstract

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.

Par-1 controls the composition and growth of cortical actin caps during Drosophila embryo cleavage

“…This cap growth defect resembled that revealed by Moe-ABD-GFP imaging in dia RNAi embryos ( Fig. 3 A) and Arp3 RNAi embryos (Zhang et al, 2018).…”

“…To assess actomyosin borders, we imaged Zipper (Zip)-GFP (nonmuscle myosin heavy chain) expressed from a homozygous viable GFP-trap allele. During early cortical divisions in control RNAi embryos, Zip-GFP first accumulated to broad domains around each cap, and these borders then thinned and ingressed at the basal tips of metaphase furrows (Zhang et al, 2018; Fig. S3 B).…”

“…The actin caps and actomyosin borders expand and meet as distinct cortical domains. Each actin cap continues its centrifugal growth but then bends inward through buckling and swelling to form a domeshaped compartment with a narrowed actomyosin network lining its basal rim (Zhang et al, 2018). Remarkably, metaphase compartments can form independently of myosin activity (Royou et al, 2004), with growth of the actin cap against residual components of its border sufficing for cortical buckling (Zhang et al, 2018).…”

Polarity protein distribution on the metaphase furrow regulates hexagon dominated plasma membrane organization in syncytialDrosophilaembryos

“…The actin caps are formed in interphase of syncytial division cycles and expand to form furrows in prophase and metaphase. Arp2/3 activity is needed for cap expansion followed by Myosin II which leads to cap buckling for the formation of furrows (Stevenson et al , 2002; Zhang et al , 2018). Also Anillin-Pnut networks have been found to play a redundant function to Myosin II in furrow initiation (Zhang et al , 2018).…”

“…Arp2/3 activity is needed for cap expansion followed by Myosin II which leads to cap buckling for the formation of furrows (Stevenson et al , 2002; Zhang et al , 2018). Also Anillin-Pnut networks have been found to play a redundant function to Myosin II in furrow initiation (Zhang et al , 2018). Septins have also been found crucial for bundling actin into curved bundles in cellularization (Mavrakis et al , 2014).…”