The mechanism of evagination of imaginal discs of Drosophila melanogaster

Fristrom, Dianne; Chihara, Charles S.

doi:10.1016/0012-1606(78)90261-0

Cited by 59 publications

(26 citation statements)

References 8 publications

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“…The existence of stress in the wing pouch might play a role in polarizing mechanics for subsequent changes (for example, when the tissue acquires its 3D shape, a process known as evagination). Polarized stress and polarized MyoII might impact on the extension of the whole pouch along the proximo-distal axis, which proceeds during evagination and is also thought to depend on cell exchanges (Condic et al, 1991;Fristrom, 1976).…”

Section: Research Articlementioning

confidence: 99%

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

2013

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Organismal development is under genetic control. Ultimately, mechanical forces shape embryos. If we want to understand the precise regulation of size and shape in animals, we must dissect how forces are distributed in developing tissues, and how they drive cell behavior to shape organs. This has not been addressed fully in the context of growing tissues. As cells grow and divide, they exert a pressure on their neighbors. How these local stresses add up or dissipate as the tissue grows is an unanswered question. We address this issue in the growing wing imaginal disc of Drosophila larvae, the precursor of the adult wing. We used a quantitative approach to analyze the strains and stresses of cells of the wing pouch, and found a global pattern of stress whereby cells in the periphery of the tissue are mechanically stretched and cells in the center are compressed. This pattern has important consequences on cell shape in the wing pouch: cells respond to it by polarizing their acto-myosin cortex, and aligning their divisions with the main axis of cell stretch, thereby polarizing tissue growth. Ectopic perturbations of tissue growth by the Hippo signaling pathway reorganize this pattern in a non-autonomous manner, suggesting a synergy between tissue mechanics and growth control during wing disc morphogenesis.

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Section: Research Articlementioning

confidence: 99%

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

2013

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“…In the fly wing, the Fat/Dachsous/Four-jointed (Ft/Ds/Fj) module aligns an apical non-centrosomal MT network (Fristrom and Fristrom, 1975;Eaton et al, 1996;Turner and Adler, 1998;Harumoto et al, 2010). The graded expression of Fj and Ds produces a slight excess of Ft activity on the proximal and Ds activity on the distal side of each cell (Yang et al, 2002;Ma et al, 2003;Ambegaonkar et al, 2012;Bosveld et al, 2012;Brittle et al, 2012) (Fig.…”

Section: Introductionmentioning

confidence: 99%

Prickle/spiny-legs isoforms control the polarity of the apical microtubule network in planar cell polarity

et al. 2014

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Microtubules (MTs) are substrates upon which plus-and minus-end directed motors control the directional movement of cargos that are essential for generating cell polarity. Although centrosomal MTs are organized with plus-ends away from the MT organizing center, the regulation of non-centrosomal MT polarity is poorly understood. Increasing evidence supports the model that directional information for planar polarization is derived from the alignment of a parallel apical network of MTs and the directional MT-dependent trafficking of downstream signaling components. The Fat/Dachsous/Fourjointed (Ft/Ds/Fj) signaling system contributes to orienting those MTs. In addition to previously defined functions in promoting asymmetric subcellular localization of 'core' planar cell polarity (PCP) proteins, we find that alternative Prickle (Pk-Sple) protein isoforms control the polarity of this MT network. This function allows the isoforms of Pk-Sple to differentially determine the direction in which asymmetry is established and therefore, ultimately, the direction of tissue polarity. Oppositely oriented signals that are encoded by oppositely oriented Fj and Ds gradients produce the same polarity outcome in different tissues or compartments, and the tissue-specific activity of alternative Pk-Sple protein isoforms has been observed to rectify the interpretation of opposite upstream directional signals. The control of MT polarity, and thus the directionality of apical vesicle traffic, by Pk-Sple provides a mechanism for this rectification.

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“…This mechanism was suggested by Fristrom (1976) for leg disc elongation during evagination, and also by Waddington for anteroposterior elongation of gastrulating presumptive mesoderm in amphibia (Waddington 1962, p. 176). Thus we use the general term "growth pattern", to include all these morphogenetic mechanisms, rather than specifying the orientation of mitotic division.…”

Section: Discussionmentioning

confidence: 84%

Pleiotropic effects in the four jointed mutant of Drosophila melanogaster.

Tokunaga¹,

Sizemore²,

Michinomae³

et al. 1982

The Japanese journal of genetics

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Studies of the adult morphology of male D. 'inelanogaster suggest that a shortening of body parts is the common aspect of the pleiotropic effects of f j (four jointed tarsi) on the development of the leg, wing, scutellum, distal parts of antenna, and one of three tergite segments measured.In the scutellum and distal antenna the only detected effect of fj is overall shortening, whereas local effects appear in leg and wing. Shortening of the leg is maximal (44%) at the proximal tarsal segments and absent at the distal two, confirming earlier studies. In the wing, total length is reduced 10% and maximum shortening (50%) occurs in the area between the anterior (ACV) and posterior (PCV) cross veins, while the proximal longitudinal veins are longer or unchanged. The effect of f j on wing width is small. Observations on cell density and bristle spacing also indicate that the strongest effect of f j is in the central area, between the ACV and PCV. We interpret the primary effect of f j to be a general reduction in the longitudinal growth pattern of many different imaginal discs. Secondary effects in the leg include a change in tarsal segmentation, followed by a bristle pattern change. In the wing, the angle of veins, bristle pattern on the subcosta vein, positions of ACV and PCV, and cell density variations are secondary effect of f j. A decrease in cell density on the wing surface between ACV and PCV may be related to a final stretching of wing tissue after the process of vein formation. Local effects are not seen in other discs which lack sequential regional patterning mechanisms emphasizing the effects of general shortening. The similarities in developmental aspects between leg and wing are discussed in relation to homoeotic changes by certain mutants.

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The mechanism of evagination of imaginal discs of Drosophila melanogaster

Cited by 59 publications

References 8 publications

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

Prickle/spiny-legs isoforms control the polarity of the apical microtubule network in planar cell polarity

Pleiotropic effects in the four jointed mutant of Drosophila melanogaster.

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