Abstract:Pulsed actomyosin contractility underlies diverse modes of tissue morphogenesis, but the underlying mechanisms remain poorly understood. Here, we combine quantitative imaging with genetic perturbations to identify a core mechanism for pulsed contractility in early C. elegans embryos. We show that pulsed accumulation of actomyosin is governed by local control of assembly and disassembly downstream of RhoA. Pulsed activation and inactivation of RhoA precede, respectively, accumulation and disappearance of actomy… Show more
“…The integrated intensities of cortical GFP::ANI-1(AH-PH) during early and late prophase were significantly greater in air-1(RNAi) zygotes than in spd-5(RNAi) zygotes ( Figure 3C). GFP::ANI-1(AH-PH) has been used to visualize pulsed activation and inactivation of RHO-1 at the cortex (Michaux et al, 2018;Nishikawa et al, 2017). Consistent with the previous observations, pulsatile behavior of GFP::ANI-1(AH-PH) was observed during early prophase in air-1(RNAi) zygotes and spd-5(RNAi) zygotes ( Figures 3A and 3B).…”
Section: Aurora-a Inhibits Excitation Of Rho-1 To Suppress Centrosomesupporting
Highlights d Aurora-A around centrosomes locally interferes cortical actomyosin contractility d Aurora-A later mediates global actomyosin disassembly to facilitate symmetry breaking d Translocation of Aurora-A to the cortex is sufficient to trigger symmetry breaking d Aurora-A induces symmetry breaking independently of its roles in centrosome maturation
“…The integrated intensities of cortical GFP::ANI-1(AH-PH) during early and late prophase were significantly greater in air-1(RNAi) zygotes than in spd-5(RNAi) zygotes ( Figure 3C). GFP::ANI-1(AH-PH) has been used to visualize pulsed activation and inactivation of RHO-1 at the cortex (Michaux et al, 2018;Nishikawa et al, 2017). Consistent with the previous observations, pulsatile behavior of GFP::ANI-1(AH-PH) was observed during early prophase in air-1(RNAi) zygotes and spd-5(RNAi) zygotes ( Figures 3A and 3B).…”
Section: Aurora-a Inhibits Excitation Of Rho-1 To Suppress Centrosomesupporting
Highlights d Aurora-A around centrosomes locally interferes cortical actomyosin contractility d Aurora-A later mediates global actomyosin disassembly to facilitate symmetry breaking d Translocation of Aurora-A to the cortex is sufficient to trigger symmetry breaking d Aurora-A induces symmetry breaking independently of its roles in centrosome maturation
“…We find that the active RhoA nullcline is nearly vertical and inconsistent with actin behaving as a negative regulator of RhoA. Note that this does not exclude the general possibility of negative feedback between actin and RhoA (Robin et al, 2016), but suggests that the C. elegans cortex is normally operating in a regime where no such negative feedback is accessed. While the detailed mechanism as well as the kinetic interactions that underlie RhoA pulsation in C. elegans remain to be determined, the RhoGEF ect-2 is involved and the system appears to undergo spatiotemporal oscillations in the absence of negative feedback between actin and RhoA.10.7554/eLife.19595.013Figure 3.Active RhoA exhibits pulsatory dynamics under conditions of reduced myosin activity.( A,B ) AHPH::GFP (green) and NMY-2::RFP (magenta) in ( A ) a representative let-502 RNAi and ( B ) a representative nmy-2 RNAi embryo.…”
The actomyosin cell cortex is an active contractile material for driving cell- and tissue morphogenesis. The cortex has a tendency to form a pattern of myosin foci, which is a signature of potentially unstable behavior. How a system that is prone to such instabilities can rveliably drive morphogenesis remains an outstanding question. Here, we report that in the Caenorhabditis elegans zygote, feedback between active RhoA and myosin induces a contractile instability in the cortex. We discover that an independent RhoA pacemaking oscillator controls this instability, generating a pulsatory pattern of myosin foci and preventing the collapse of cortical material into a few dynamic contracting regions. Our work reveals how contractile instabilities that are natural to occur in mechanically active media can be biochemically controlled to robustly drive morphogenetic events.DOI:
http://dx.doi.org/10.7554/eLife.19595.001
“…Dynamic actomyosin behaviors like those observed here are regulated through RhoA activation and inhibition (39)(40)(41). RhoA is a small GTPase activated by guanine nucleotide exchange factors (GEFs) and inhibited by GTPase-activating proteins (GAPs) (42,43 (17)(18)(19)(20).…”
29Interactions in which individuals benefit others at a cost to themselves are rife within the 30 animal kingdom 1 , from stalk cells in slime mold fruiting bodies 2 to social insect colonies where 31 sterile workers live for the queen 3 . The development of an egg cell occurs within similarly self-32 sacrificing communes. Across species, oocytes develop within cysts alongside nurse-like germ 33 cells; a key juncture in oogenesis occurs when these sister cells transport their cytoplasm to the 34 oocyte prior to fertilization 4,5 . As a result, the oocyte grows as its sister cells regress and die 6 . 35 Long observed in insects, recent work shows that development of the mammalian egg cell occurs 36 through similar intercellular transport processes 7,8 . Although critical for fertility and embryonic 37 life, the biological and physical mechanisms underlying such altruistic fluid transport remain 38 poorly understood, owing to a lack of time-resolved quantitative data. Here, we combined ex vivo 39 live imaging of germline cysts with mathematical modeling to investigate the dynamics and 40 mechanisms that enable directional and complete cytoplasmic transport in Drosophila 41 melanogaster egg chambers. We discovered that during 'nurse cell dumping', most cytoplasm is 42 transported into the oocyte independently of changes in myosin-II contractility, with dynamics 43 predicted by Young-Laplace's law, suggesting pressure-driven transport induced by baseline cell 44 surface tension. A minimal flow network model inspired by the famous two-balloon experiment 45 correctly predicts transport directionality and time scale. Long thought to trigger transport 46 through 'squeezing' 9,10 , increased actomyosin contractility is required only once cell volume is 47 reduced by ~75%, in the form of cell peristaltic contractile waves that permit continued flow. Our 48 work thus demonstrates how biological and physical mechanisms cooperate to enable proper cell 49 and tissue level behaviours during a conserved act of cytoplasmic transport in early development. 50 51 Main text 52The Drosophila oocyte develops within an egg chamber, a multicellular structure that comprises a 53 germline cyst of 16 cells that are interconnected through intercellular bridges called ring canals and 54 covered by an epithelium (Fig. 1a) [11][12][13] . After the oocyte grows to ~50% of the egg chamber's volume, all 55 15 sister germ cells, called nurse cells, transport the entirety of their contents directionally into the oocyte 56 in a process called 'nurse cell (NC) dumping'; with a diameter of ~10 µm, ring canals are large enough to 57 permit passage of most cytoplasmic contents ( Fig. 1b; Extended Data Fig. 1a; Supplementary Video 1) 14 . 58 It is thought that NC dumping is driven by global cortical contractile forces generated through interactions 59 of non-muscle myosin II (myosin) with actin filaments (henceforth actomyosin), i.e. through an increase in 60 pressure, cytoplasm is 'squeezed' out of the NCs and into the oocyte 9,10 . While mutants in ...
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