Zygotically controlled F-actin establishes cortical compartments to stabilize furrows duringDrosophilacellularization

Abstract

Cortical compartments partition proteins and membrane at the cell surface to define regions of specialized function. Here we ask how cortical compartments arise along the plasma membrane furrows that cellularize the early Drosophila embryo, and investigate the influence that this compartmentalization has on furrow ingression. We find that the zygotic gene product Nullo aids the establishment of discrete cortical compartments, called furrow canals, which form at the tip of incipient furrows. Upon nullo loss-of-function, proteins that are normally restricted to adjacent lateral regions of the furrow, such as Neurotactin and Discs large, spread into the furrow canals. At the same time, cortical components that should concentrate in furrow canals, such as Myosin 2 (Zipper) and Anillin (Scraps), are missing from some furrows. Depletion of these cortical components from the furrow canal compartments precipitates furrow regression. Contrary to previous models, we find that furrow compartmentalization does not require cell-cell junctions that border the furrow canals. Instead, compartmentalization is disrupted by treatments that reduce levels of cortical F-actin. Because the earliest uniform phenotype detected in nullo mutants is reduced levels of F-actin at furrow canals, we propose that Nullo compartmentalizes furrows via its regulation of Factin, thus stabilizing furrows and insuring their ingression to complete cellularization. Supplementary material available online at

Maternal and zygotic requirements for src64 during Drosophila cellularization

“…This membrane is continuous, folding back on itself, forming stable furrow canals at the cellularization front (Fullilove and Jacobson, 1971;Lecuit and Wieschaus, 2000). F-actin and myosin II surround the furrow canals, forming a network of contractile microfilament rings (Schejter and Wieschaus, 1993;Sokac and Wieschaus, 2008b;Warn and Robert-Nicoud, 1990;Young et al, 1991). During early cellularization, before the cellularization front passes the nuclei, contractile tension in the microfilament network maintains uniform invagination of the cellularization front.…”

The Drosophila MAST kinase Drop out is required to initiate membrane compartmentalisation during cellularisation and regulates dynein-based transport

“…Although we cannot exclude the possibility that bnk might play a role in later defects associated with dop mutations, the primary defect in dop mutants concerned the lack of regular F-actinrich furrows during the onset of cellularisation. Another early zygotic gene, nullo, is required for the proper recruitment of F-actin during furrow canal formation (Sokac and Wieschaus, 2008b). Nullo and the actin regulator RhoGEF2 have been proposed to act in parallel pathways controlling processes that are distinct but both essential for F-actin network formation during the establishment of the furrow canal (Grosshans et al, 2005).…”

“…Cortical asymmetry becomes evident by accumulation of proteins including F-actin and Myosin II, which mark the sites where cleavage furrows invaginate (Sokac and Wieschaus, 2008b). These incipient cleavage furrows mature to form furrow canals that are stabilised by actin/myosin, the actin regulators RhoGEF2, Rho1 and Diaphanous (Dia), and additional regulatory proteins including Slow as Molasses (Slam), Septins, Nullo and Patj (Hunter and Wieschaus, 2000;Lecuit et al, 2002;Grosshans et al, 2005;Sokac and Wieschaus, 2008b;Wenzl et al, 2010). Basal adherens junctions (bAJs) form apical to the furrow canal and move inward with the furrows (Müller and Wieschaus, 1996;Hunter and Wieschaus, 2000).…”

Modelling and Image Processing of Constriction and Proliferation in the Gastrulation Process of Drosophila melanogaster

“…Our numerical experiments made during the time lag observed through the microscopic imaging without proliferation suggest that our model adequately simulates thge in-vivo cell behaviour. In a first part, we present image processing techniques and results obtained by applying them on gastrulation microscopic recording of Drosophila melanogaster embryo from [2][3][4][5][6]. In a second part, we describe the biomechanical model of streak formation and the third Section will be devoted to the presentation of numerical simulations confronted to real images of the first invagination stage of the gastrulation.…”

“…Each force is equal to a coefficient (e.g. the physical pressure) times the length of the wall on which it is exerted 2) If we suppose that the initial cell configuration is in an equilibrium state, we calculate an admissible set of parameters values respecting this equilibrium 3) Then, we leave the cell system evolve depending on the energetic balance r u l i n g t h e c y t o s k e l e t o n a p i c a l polymerization [4][5][6] c o n t r o l l e d b y a s p e c i f i c g e n e t i c regulatory n e t w o r k c o m p r i z i n g e s s e n t i a l l y c o n c e r t i n a ( c t a ), actin, myosin, Rho and RhoGEF genes [7][8][9][10], by choosing a small time step, by updating sequentially each cell and by calculating their displacements respecting the no-overlapping rule. At each step we update the cell common walls by supposing that cell contacts are close, ensured between cells by cadherins and gap junctions [11,12], and with the extracellular matrix by integrins and adhesins.…”