scholarly journals Ecdysone regulates the Drosophila imaginal disc epithelial barrier, determining the duration of regeneration checkpoint delay

2020 ◽  
Author(s):  
Danielle DaCrema ◽  
Rajan Bhandari ◽  
Faith Karanja ◽  
Ryunosuke Yano ◽  
Adrian Halme

AbstractRegeneration of Drosophila imaginal discs, larval precursors to adult tissues, produces a systemic response, a regeneration checkpoint that coordinates regenerative growth with developmental progression. This regeneration checkpoint is coordinated by the release of the relaxin-family peptide Dilp8 from regenerating tissues. Secreted Dilp8 protein can be detected within the imaginal disc lumen. The disc epithelium separates from the lumen from the larval hemolymph and the targets for Dilp8 activity in the brain and prothoracic gland. Here we demonstrate that the imaginal disc epithelial barrier limits Dilp8 signaling and checkpoint delay. We also observe that the wing imaginal disc barrier becomes more restrictive during development, becoming impermeable only at end of the final larval instar. This change in barrier permeability is driven by the steroid hormone ecdysone and correlates with changes in localization of Coracle, a component of the septate junctions that is required for the late, impermeable epithelial barrier. Based on these observations, we propose that the imaginal disc epithelial barrier regulates the duration of the regenerative checkpoint, providing a mechanism by which tissue function can signal the completion of regeneration.Summary StatementEcdysone signaling directs the Drosophila third instar imaginal disc epithelial barrier to mature, becoming more restrictive. This mature barrier limits Dilp8 signaling and determines the duration of the regeneration checkpoint.

Development ◽  
2021 ◽  
Vol 148 (6) ◽  
Author(s):  
Danielle DaCrema ◽  
Rajan Bhandari ◽  
Faith Karanja ◽  
Ryunosuke Yano ◽  
Adrian Halme

ABSTRACT Regeneration of Drosophila imaginal discs, larval precursors to adult tissues, activates a regeneration checkpoint that coordinates regenerative growth with developmental progression. This regeneration checkpoint results from the release of the relaxin-family peptide Dilp8 from regenerating imaginal tissues. Secreted Dilp8 protein is detected within the imaginal disc lumen, in which it is separated from its receptor target Lgr3, which is expressed in the brain and prothoracic gland, by the disc epithelial barrier. Here, we demonstrate that following damage the imaginal disc epithelial barrier limits Dilp8 signaling and the duration of regeneration checkpoint delay. We also find that the barrier becomes increasingly impermeable to the transepithelial diffusion of labeled dextran during the second half of the third instar. This change in barrier permeability is driven by the steroid hormone ecdysone and correlates with changes in localization of Coracle, a component of the septate junctions that is required for the late-larval impermeable epithelial barrier. Based on these observations, we propose that the imaginal disc epithelial barrier regulates the duration of the regenerative checkpoint, providing a mechanism by which tissue function can signal the completion of regeneration.


2015 ◽  
Author(s):  
Jacob S. Jaszczak ◽  
Jacob B. Wolpe ◽  
Anh Q. Dao ◽  
Adrian Halme

Mechanisms that coordinate the growth of different tissues during development are essential for producing adult animals with proper organ proportion. Here we describe a pathway through which tissues communicate with each other to coordinate growth. DuringDrosophila melanogasterlarval development, damage to imaginal discs activates a regeneration checkpoint that produces both a delay in developmental timing and slows the growth of undamaged tissues, coordinating regeneration of the damaged tissue with developmental progression and overall growth. Both developmental delay and growth control are mediated by secretion of the insulin/relaxin family peptide Dilp8 from regenerating tissues. Here we demonstrate that Dilp8-dependent growth coordination between regenerating and undamaged tissues, but not developmental delay, requires the activity of nitric oxide synthase (NOS) in the prothoracic gland. NOS limits the growth of undamaged tissues by reducing ecdysone biosynthesis, a requirement for imaginal disc growth during both the regenerative checkpoint and normal development. Therefore, NOS activity in the prothoracic gland translates information about the growth status of individual tissues into coordinated tissue growth through the regulation of endocrine signals.


2015 ◽  
Author(s):  
Jacob S. Jaszczak ◽  
Jacob B. Wolpe ◽  
Rajan Bhandari ◽  
Rebecca G. Jaszczak ◽  
Adrian Halme

Damage to Drosophila melanogaster imaginal discs activates a regeneration checkpoint that 1) extends larval development and 2) coordinates the regeneration of the damaged disc with the growth of undamaged discs. These two systemic responses to damage are both mediated by Dilp8, a member of the insulin/IGF/relaxin family of peptide hormones, which is released by regenerating imaginal discs. Growth coordination between regenerating and undamaged imaginal discs is dependent on Dilp8 activation of NOS in the prothoracic gland (PG), which slows the growth of undamaged discs by limiting ecdysone synthesis. Here we demonstrate that the Drosophila relaxin receptor homologue Lgr3, a leucine-rich repeat-containing G-protein coupled receptor, is required for Dilp8-dependent growth coordination and developmental delay during the regeneration checkpoint. Lgr3 regulates these responses to damage via distinct mechanisms in different tissues. Using tissue-specific RNAi disruption of Lgr3 expression, we show that Lgr3 functions in the PG upstream of nitric oxide synthase (NOS), and is necessary for NOS activation and growth coordination during the regeneration checkpoint. When Lgr3 is depleted from neurons, imaginal disc damage no longer produces either developmental delay or growth inhibition. To reconcile these discrete tissue requirements for Lgr3 during regenerative growth coordination, we demonstrate that Lgr3 activity in the both the CNS and PG is necessary for NOS activation in the PG following damage. Together, these results identify new roles for a relaxin receptor in mediating damage signaling to regulate growth and developmental timing.


Development ◽  
1975 ◽  
Vol 33 (2) ◽  
pp. 487-498
Author(s):  
Andreas Dübendorfer ◽  
Glen Shields ◽  
James H. Sang

Embryos of Drosophila melanogaster, 6–8 h after oviposition, were dissociated and the cells cultured in vitro. Besides larval cell types, imaginal disc cells, assembled and growing in bloated monolayered vesicles, were obtained. The cells of these vesicles become competent to differentiate adult structures when treated with α-ecdysone or ecdysterone in vitro. Recognizable patterns of the adult fly are not formed though. If metamorphosis of imaginal cell vesicles from in vitro-cultures is induced in vivo by transplantation into host larvae of various ages within the third larval instar, recognizable patterns can differentiate provided the host larva does not metamorphose prior to 2 days after transplantation. The frequency of specific patterns in the implants can be increased by providing 9 days of culture in vivo (adult host flies) before metamorphosis. Passage through the third larval instar is not essential for these cells to produce identifiable patterns since culture in adult flies alone can achieve this. The quality of the differentiated pattern is not correlated with the extent of cell proliferation in the cultured tissues. The problem of pattern specification in vitro and in vivo is discussed.


1997 ◽  
Vol 3 (S2) ◽  
pp. 1129-1130
Author(s):  
John Archie Pollock ◽  
Bejon T. Maneckshana ◽  
Teresa E. Leonardo

The compound eye of the fruit fly, Drosophila melanogaster, is composed of a highly ordered array of facets (FIG. 1), each containing a precise set of neurons and supporting cells. The eye arises during the third larval instar from an undifferentiated epithelium, the eye imaginai disc, which is connected to the brain via the optic stalk (FIG. 2). During eye development, movement of the morphogenetic furrow, progressive recruitment of specific cell types and the growth of photoreceptor axons into the brain are each dynamic processes that are routinely studied indirectly in fixed tissues. While stereotyped development and the ‘crystalline’ like structure of the eye facilitates this analysis, certain experiments are hindered by the inability to observe developmental processes as they occur. To overcome this limitation, we have combined organ culture with advanced microscopy tools to enable the observation of eye development in living tissue.


Nature ◽  
1968 ◽  
Vol 220 (5168) ◽  
pp. 706-707 ◽  
Author(s):  
D. B. CARLISLE ◽  
P. E. ELLIS
Keyword(s):  

2019 ◽  
Author(s):  
Divya Rao ◽  
Satoshi Kojima ◽  
Raghav Rajan

ABSTRACTMany self-initiated, learned, motor sequences begin by repeating a simple movement, like ball-bouncing before a tennis serve, and this repetition is thought to represent motor preparation. Do these simple movements provide real-time sensory feedback used by the brain for getting ready or do they simply reflect internal neural preparatory processes? Here, we addressed this question by examining the introductory notes (INs) that zebra finches repeat before starting their learned song sequence. INs progress from a variable initial state to a stereotyped final state before each song and are thought to represent motor preparation before song. Here, we found that the mean number of INs before song and the progression of INs to song were not affected by removal of two sensory feedback pathways (auditory and proprioceptive). In both feedback-intact and feedback-deprived birds, the presence of calls (other non-song vocalizations), just before the first IN, was correlated with fewer INs before song and an initial state closer to song. Finally, the initial IN state correlated with the time to song initiation. Overall, these results show that INs do not provide real-time sensory feedback for preparing the motor system. Rather, repetition of INs, and possibly, other such simple movements, may reflect the “current” state of internal neural preparatory processes involved in getting the brain ready to initiate a learned movement sequence.SUMMARY STATEMENTThe number and progression of introductory notes to song in the zebra finch are not affected by removal of sensory feedback.


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