The endocycle restores tissue tension in the Drosophila abdomen post wound repair

Losick, Vicki P.; Duhaime, Levi G.

doi:10.1016/j.celrep.2021.109827

Cited by 7 publications

(10 citation statements)

References 55 publications

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“…The averaged, MRLC-mCherry intensities were slightly higher in the AS, and the relative upregulation of ≈1.4-fold in AS and 1.2-fold in the epidermis was significantly different ( Figure 6C ). Using a phospho-specific myosin antibody (P-Myo) ( Losick and Duhaime, 2021 ), we confirmed the developmental upregulation of active myosin both in AS and in the lateral epidermal cells ( Supplementary Figure S3 ). P-Myo staining was comparable in AS and the lateral epidermal cells at the elliptical stage ( Supplementary Figure S3B ).…”

Section: Resultsmentioning

confidence: 56%

The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure

Zhang

et al. 2022

Front. Cell Dev. Biol.

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Dorsal closure is a prominent morphogenetic process during Drosophila embryogenesis, which involves two epithelial tissues, that is, the squamous amnioserosa and the columnar lateral epidermis. Non-muscle myosin II-driven constriction in the amnioserosa leads to a decrease in the apical surface area and pulls on the adjacent lateral epidermis, which subsequently moves dorsally. The pull by the amnioserosa becomes obvious in an elongation of the epidermal cells, especially of those in the first row. The contribution of the epidermal cell elongation has remained unclear to dorsal closure. Cell elongation may be a mere passive consequence or an active response to the pulling by the amnioserosa. Here, we found that the lateral epidermis actively responds. We analyzed tensions within tissues and cell junctions by laser ablation before and during dorsal closure, the elliptical and dorsal closure stages, respectively. Furthermore, we genetically and optochemically induced chronic and acute cell contraction, respectively. In this way, we found that tension in the epidermis increased during dorsal closure. A correspondingly increased tension was not observed at individual junctions, however. Junctional tension even decreased during dorsal closure in the epidermis. We strikingly observed a strong increase of the microtubule amount in the epidermis, while non-muscle myosin II increased in both tissues. Our data suggest that the epidermis actively antagonizes the pull from the amnioserosa during dorsal closure and the increased microtubules might help the epidermis bear part of the mechanical force.

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Section: Resultsmentioning

confidence: 56%

The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure

Zhang

et al. 2022

Front. Cell Dev. Biol.

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“…S4A; Fig. 5A) (Losick and Duhaime, 2021). This myosin organization is disrupted in 40-day-old animals, where Sqh-GFP becomes more diffuse and dispersed across the epithelium (Fig.…”

Section: Inhibition Of Cell Fusion With Age Does Not Significantly Al...mentioning

confidence: 86%

“…The abdomen of the fruit fly also needs to be able to stretch and bend in response to changing physiological and environmental conditions. We recently discovered that epithelial tension contributes to the ability of the male fly to efficiently bend its abdomen (Losick and Duhaime, 2021). Therefore, we assayed whether syncytia also arose with age in the ventral epithelium of the male fly.…”

Section: Drosophila Abdominal and Epithelial Mechanics Decline With A...mentioning

confidence: 99%

“…Epithelial tension can be inferred by measuring the relative recoil velocity following a laser ablation cut of the epithelial non-muscle myosin II protein network via expression of the Drosophila myosin regulatory light chain (called Sqh) fused to GFP (Sqh-GFP) (Shivakumar and Lenne, 2016). As we reported previously, the relative recoil velocity was determined by ablating a 1 µm line through the Sqh-GFP-enriched region in the abdominal epithelium (Losick and Duhaime, 2021). This led to an initial mean recoil velocity of 14.2 µm/s in epithelium from young 7-day-old animals, similar to our previous results demonstrating that adult epithelium is under tension (Fig.…”

Section: Drosophila Abdominal and Epithelial Mechanics Decline With A...mentioning

confidence: 99%

“…Consequently, the velocity of organismal movement is used as an indicator of healthspan in model organisms (Hahm et al, 2015). We recently discovered that the adult Drosophila abdominal epithelium is under tension, which is required for efficient bending in male fruit flies mimicking their copulation behavior (Losick and Duhaime, 2021). Multinucleated polyploid cells have been found to arise during both wound healing and aging in Drosophila (Galko and Krasnow, 2004;Losick et al, 2013;Scherfer et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Epithelial mechanics are maintained by inhibiting cell fusion with age in Drosophila

Dehn,

Duhaime,

Gogna

et al. 2023

Journal of Cell Science

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A characteristic of normal aging and age-related diseases is the remodeling of a tissue's cellular organization through polyploid cell growth. Polyploidy arises from an increase in nuclear ploidy or the number of nuclei per cell. However, it is not known whether age-induced polyploidy is an adaption to stressors or a precursor to degeneration. Here, we find that the adult fruit fly's abdominal epithelium becomes polyploid with age through generation of multinucleated cells by cell fusion. Inhibition of fusion does not improve the fly's lifespan, but does enhance its biomechanical fitness, a measure of the animal's healthspan. Remarkably, Drosophila can maintain their epithelial tension and abdominal movements with age when cell fusion is inhibited. Epithelial cell fusion also appears to be dependent on a mechanical cue as knockdown of Rho kinase, E-cadherin, or -catenin are sufficient to induce multinucleation in young animals. Interestingly, mutations in -catenin in mice result in retina pigment epithelial multinucleation associated with macular disease. Therefore, we have discovered that polyploid cells arise by cell fusion and contribute to the decline in the animal's biomechanical fitness with age.

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Germline and Somatic Cell Syncytia in Insects

Kloc,

Tworzydło,

Szklarzewicz

2023

Results and Problems in Cell Differentiation

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The endocycle restores tissue tension in the Drosophila abdomen post wound repair

Abstract: Highlights d The endocycle upregulates NMII during wound healing d The endocycle is required, but not sufficient, to enhance epithelial tension after wound repair

Cited by 7 publications

References 55 publications

The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure

The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure

Epithelial mechanics are maintained by inhibiting cell fusion with age in Drosophila

Germline and Somatic Cell Syncytia in Insects

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