Cell cycling and patterned cell proliferation in the wing primordium of Drosophila.

Milán, Marco; Campuzano, Sonsoles; Garcı́a-Bellido, Antonio

doi:10.1073/pnas.93.2.640

Cited by 219 publications

(203 citation statements)

References 22 publications

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“…In the same way, stg expression was detected in wild-type wing discs as previously (g) vg null wing disc in which vg is overexpressed in the progeny of the cross between vg null ; UAS-vg and vg null ; ptc-GAL4 flies. Staining with anti-dE2F antibodies reveals that vg induces the expression of the dE2F protein described, 1 and was induced by ectopic vg (Figure 5c, d). Taken together our results show that ectopic vg is sufficient to induce expression of a functional dE2F transcription factor and two of its target genes dmRNR2 and stg.…”

Section: Vg and Sd Induce Proliferation Of Hela Cellsmentioning

confidence: 96%

“…BrdU and DAPI labeling of imaginal discs was performed as described. 1 Staining with rabbit antiphospho-histone H3 antibody (Upstate Biotechnology), anti-VG (gift from S Carroll), anti-dE2F1 (gift from P Leopold) anti-DIAP1 (gift from HD Ryoo and H Steller), CM1 antiactivated caspases antibodies (BD Pharmingen) and mouse anti-b-galactosidase antibody (Jackson Immuno Labs) were performed according to standard protocols.…”

Section: Histologymentioning

confidence: 99%

“…1 Wing growth is patterned by the establishment of compartments of specialized cells, marked by boundaries. The antero-posterior (A/P) compartments are established early during embryogenesis under the control of the engrailed (en) selector gene that regulates the decapentaplegic (dpp) morphogen.…”

Section: Introductionmentioning

confidence: 99%

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The Drosophila wing differentiation factor Vestigial–Scalloped is required for cell proliferation and cell survival at the dorso-ventral boundary of the wing imaginal disc

et al. 2003

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Links between genes involved in development, proliferation and apoptosis have been difficult to establish. In the Drosophila wing disc, the vestigial (vg) and the scalloped (sd) gene products dimerize to form a functional transcription factor. Ectopic expression of vg in other imaginal discs induces outgrowth and wing tissue specification. We investigated the role of the VG-SD dimer in proliferation and showed that vg antagonizes the effect of dacapo, the cyclin-cdk inhibitor. Moreover, ectopic vg drives cell cycle progression and in HeLa cultured cells, the VG-SD dimer induces cell proliferation per se. In Drosophila, ectopic vg induces expression of dE2F1 and its targets dRNR2 and string. In addition vg, but not dE2F1, interacts with and induces expression of dihydrofolate reductase (DHFR). Moreover, a decrease in VG or addition of aminopterin, a specific DHFR inhibitor, shift the dorso-ventral boundary cells of the disc to a cell death sensitive state that is correlated with reaper induction and DIAP1 downregulation. This indicates that vg in interaction with dE2F1 and DHFR is a critical player for both cell proliferation and cell survival in the presumptive wing margin area.

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Section: Vg and Sd Induce Proliferation Of Hela Cellsmentioning

confidence: 96%

Section: Histologymentioning

confidence: 99%

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The Drosophila wing differentiation factor Vestigial–Scalloped is required for cell proliferation and cell survival at the dorso-ventral boundary of the wing imaginal disc

et al. 2003

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“…A fruit fly, Drosophila melanogaster, has been an invaluable model of development in general and organogenesis in particular (6,7). Below, we focus on the question of growth control (8,9) in the context of a wing imaginal disc (7), which is the larval precursor of the adult wing. We point out that nonuniform growth in a layer of cells that adhere to each other (as is the case for imaginal discs) leads to accumulation of mechanical stress.…”

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confidence: 99%

Mechanical feedback as a possible regulator of tissue growth

Shraiman

2005

Proc. Natl. Acad. Sci. U.S.A.

573

517

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Regulation of cell growth and proliferation has a fundamental role in animal and plant development and in the progression of cancer. In the context of development, it is important to understand the mechanisms that coordinate growth and patterning of tissues. Imaginal discs, which are larval precursors of fly limbs and organs, have provided much of what we currently know about these processes. Here, we consider the mechanism that is responsible for the observed uniformity of growth in wing imaginal discs, which persists in the presence of gradients in growth inducing morphogens in spite of the stochastic nature of cell division. The phenomenon of ''cell competition,'' which manifests in apoptosis of slowergrowing cells in the vicinity of faster growing tissue, suggests that uniform growth is not a default state but a result of active regulation. How can a patch of tissue compare its growth rate with that of its surroundings? A possible way is furnished by mechanical interactions. To demonstrate this mechanism, we formulate a mathematical model of nonuniform growth in a layer of tissue and examine its mechanical implications. We show that a clone growing faster or slower than the surrounding tissue is subject to mechanical stress, and we propose that dependence of the rate of cell division on local stress could provide an ''integral-feedback'' mechanism stabilizing uniform growth. The proposed mechanism of growth control is not specific to imaginal disc growth and could be of general relevance. Several experimental tests of the proposed mechanism are suggested.Drosophila melanogaster ͉ imaginal disc ͉ mechanics ͉ stress U nderstanding the principles and mechanisms involved in animal and plant development remains an outstanding challenge for modern biology (1, 2). Among the fundamental problems is the problem of understanding how organisms (or organs and body parts) coordinate their growth with internal patterning to achieve correct size and proportions (3-5). A fruit fly, Drosophila melanogaster, has been an invaluable model of development in general and organogenesis in particular (6, 7). Below, we focus on the question of growth control (8, 9) in the context of a wing imaginal disc (7), which is the larval precursor of the adult wing. We point out that nonuniform growth in a layer of cells that adhere to each other (as is the case for imaginal discs) leads to accumulation of mechanical stress. This stress may provide cells with a feedback signal, regulating cell division and insuring stable and uniform growth of tissue. To describe this process quantitatively, we formulate and analyze a mathematical model of mechanical deformation in growing tissue. We show that the proposed mechanical feedback model could naturally explain certain salient features of growth in imaginal discs, such as ''cell competition'' (6, 10, 11), and suggest experiments that would directly test the model.The possible role of mechanical interactions in growth has been suggested, most explicitly in the context of plant development (12-15). Ho...

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“…Studies of the growth rates of mosaic patches and the rates of accumulation of BrdU label in, and disappearance from, wing imaginal disc chromosomes have demonstrated an intrinsic variation in the cell-cycle rate (Milan et al, 1996a;Tsuji and Tobari, 1980). However, the analyses performed in these works failed to show the range of cell-cycle rate variation in the tissues considered.…”

Section: Dispersion Of Cell-cycle Ratesmentioning

confidence: 99%

Analysis of cell proliferation in Drosophila wing imaginal discs using mosaic clones

Dubatolova

Omelyanchuk

2004

Heredity

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Experimental data on spatial and temporal distributions of mosaic clones in Drosophila wing imaginal disc were analyzed. Long-lived proliferation centers (PR1, PR2, and PR3) and areas with decreased proliferation activity were found in the notum region of the disc. Simulation of the growth kinetics of mosaic patches demonstrated that the cell cycle in proliferation centers PR2 and PR3 was shorter than the average cycle in the disc and in the center PR1. A nonrandom clustering of rapidly dividing cells was observed in the PR2, but not in the other cases. The reason why the cell-cycle duration and the clustering of dividing cells may not coincide is discussed in terms of the recruitment of nondividing cells into the cell cycle. The simulation of the time course of the first and second moments of the size distribution of mosaic clones allowed the variance of cellcycle progression rates to be determined and demonstrated that a model with a continuous cell-cycle rates gave a better fit to the data than the transition probability model of Smith and Martin.

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Cell cycling and patterned cell proliferation in the wing primordium of Drosophila.

Cited by 219 publications

References 22 publications

The Drosophila wing differentiation factor Vestigial–Scalloped is required for cell proliferation and cell survival at the dorso-ventral boundary of the wing imaginal disc

The Drosophila wing differentiation factor Vestigial–Scalloped is required for cell proliferation and cell survival at the dorso-ventral boundary of the wing imaginal disc

Mechanical feedback as a possible regulator of tissue growth

Analysis of cell proliferation in Drosophila wing imaginal discs using mosaic clones

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