Dataset Information

Coordination of cytoskeletal dynamics and cell behaviour during Drosophila abdominal morphogenesis.

ABSTRACT: During morphogenesis, cells exhibit various behaviours, such as migration and constriction, which need to be coordinated. How this is achieved remains elusive. During morphogenesis of the Drosophila adult abdominal epidermis, larval epithelial cells (LECs) migrate directedly before constricting apically and undergoing apoptosis. Here, we study the mechanisms underlying the transition from migration to constriction. We show that LECs possess a pulsatile apical actomyosin network, and that a change in network polarity correlates with behavioural change. Exploring the properties of the contractile network, we find that cell contractility, as determined by myosin activity, has an impact on the behaviour of the network, as well as on cytoskeletal architecture and cell behaviour. Pulsed contractions occur only in cells with intermediate levels of contractility. Furthermore, increasing levels of the small Rho GTPase Rho1 disrupts pulsing, leading to cells that cycle between two states, characterised by a junctional cortical and an apicomedial actin network. Our results highlight that behavioural change relies on tightly controlled cellular contractility. Moreover, we show that constriction can occur without pulsing, raising questions why constricting cells pulse in some contexts but not in others.

SUBMITTER: Pulido Companys P

PROVIDER: S-EPMC7132776 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Coordination of cytoskeletal dynamics and cell behaviour during <i>Drosophila</i> abdominal morphogenesis.

Pulido Companys Pau P Norris Anneliese A Bischoff Marcus M

Journal of cell science 20200330 6

During morphogenesis, cells exhibit various behaviours, such as migration and constriction, which need to be coordinated. How this is achieved remains elusive. During morphogenesis of the <i>Drosophila</i> adult abdominal epidermis, larval epithelial cells (LECs) migrate directedly before constricting apically and undergoing apoptosis. Here, we study the mechanisms underlying the transition from migration to constriction. We show that LECs possess a pulsatile apical actomyosin network, and that ...[more]

PMID: 32229579

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Project description:BACKGROUND:During Drosophila oogenesis, the follicular epithelium differentiates into several morphologically distinct follicle-cell populations. Characteristic bioelectrical properties make this tissue a suitable model system for studying connections between electrochemical signals and the organisation of the cytoskeleton. Recently, we have described stage-specific transcellular antero-posterior and dorso-ventral gradients of intracellular pH (pHi) and membrane potential (Vmem) depending on the asymmetrical distribution and/or activity of various ion-transport mechanisms. In the present study, we analysed the patterns of basal microfilaments (bMF) and microtubules (MT) in relation to electrochemical signals. RESULTS:The bMF- and MT-patterns in developmental stages 8 to 12 were visualised using labelled phalloidin and an antibody against acetylated α-tubulin as well as follicle-cell specific expression of GFP-actin and GFP-α-tubulin. Obviously, stage-specific changes of the pHi- and Vmem-gradients correlate with modifications of the bMF- and MT-organisation. In order to test whether cytoskeletal modifications depend directly on bioelectrical changes, we used inhibitors of ion-transport mechanisms that have previously been shown to modify pHi and Vmem as well as the respective gradients. We inhibited, in stage 10b, Na+/H+-exchangers and Na+-channels with amiloride, V-ATPases with bafilomycin, ATP-sensitive K+-channels with glibenclamide, voltage-dependent L-type Ca2+-channels with verapamil, Cl--channels with 9-anthroic acid and Na+/K+/2Cl--cotransporters with furosemide, respectively. The correlations between pHi, Vmem, bMF and MT observed in different follicle-cell types are in line with the correlations resulting from the inhibition experiments. While relative alkalisation and/or hyperpolarisation stabilised the parallel transversal alignment of bMF, acidification led to increasing disorder and to condensations of bMF. On the other hand, relative acidification as well as hyperpolarisation stabilised the longitudinal orientation of MT, whereas alkalisation led to loss of this arrangement and to partial disintegration of MT. CONCLUSIONS:We conclude that the pHi- and Vmem-changes induced by inhibitors of ion-transport mechanisms simulate bioelectrical changes occurring naturally and leading to the cytoskeletal changes observed during differentiation of the follicle-cell epithelium. Therefore, gradual modifications of electrochemical signals can serve as physiological means to regulate cell and tissue architecture by modifying cytoskeletal patterns.

Dataset Information

Coordination of cytoskeletal dynamics and cell behaviour during Drosophila abdominal morphogenesis.

Publications

Coordination of cytoskeletal dynamics and cell behaviour during <i>Drosophila</i> abdominal morphogenesis.

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