Pattern reorganization occurs independently of cell division during Drosophila wing disc regeneration in situ

Abstract

One of the most intriguing problems in developmental biology is how an organism can replace missing organs or portions of its body after injury. This capacity, known as regeneration, is conserved across different phyla. The imaginal discs of Drosophila melanogaster provide a particularly well-characterized model for analyzing regeneration. We have developed a unique method to study organ regeneration under physiological conditions using the imaginal discs of Drosophila. Using this method, we revisited different aspects of organ regeneration. The results presented in this report suggest that during the initial stages of regeneration, different processes occur, including wound healing, a temporary loss of markers of cell-fate commitment, and pattern reorganization. We present evidence indicating that all of these processes occur even when cell division has been arrested. Our data also suggested that Wingless is not required during the early stages of disc regeneration.epimorphic | morphallatic R egeneration allows for the replacement of missing organs or body parts when they are damaged. In 1901, Morgan (1) proposed two different regenerative models: regeneration that allows for the reconstruction of the lost structure as a result of regenerative growth and regeneration that remodels the remaining tissues without proliferation. The first model is an addon regeneration, known as epimorphic regeneration, which has been extensively studied in different organisms (2). In these animals, after the amputation of a portion of the limb, a group of differentiated cells near the injured region dedifferentiate and form the blastema (3). These cells then proliferate to reconstruct the amputated structure. In contrast, in the second model of regeneration, which is known as morphallactic regeneration, tissue remodeling and the redifferentiation of cells in the absence of proliferation occurs (4).The imaginal discs of Drosophila have been used as a classical model for the study of the genetic and molecular basis of organ regeneration (review by ref. 5). These structures give rise to the adult organs of Drosophila. The imaginal wing disc is the precursor of the wing and notum in the adult. Cells that constitute these discs begin to divide during the first larval stage and continue proliferating until the end of larval development, and it is during this time that the characteristics of the adult wings are defined (6).The standard approach used to study regeneration in Drosophila has been to grow the regenerating structures in an in vivo culture. The disc is extracted from the larva and, after removing a fragment of it, transplanted into the abdomen of an adult host where the cells proliferate but do not differentiate (7,8). The results obtained from these experiments revealed a zone of high cell proliferation on the edges of the wound, similar to the blastema that originates during limb regeneration in amphibians (9, 10). These studies suggest that the regeneration of lost structures in Drosophila is the result of regenerative grow...

During Drosophila disc regeneration, JAK/STAT coordinates cell proliferation with Dilp8-mediated developmental delay

“…In addition, the region of P3/4 samples is, indeed, overlaid with developmental wg expression; therefore, we assume that the expression of wound-induced wg would be masked in our microarray analysis. A recent study showed that the genes associated with pattern formation are temporally disrupted in damaged discs before initiating regenerative proliferation (40). In our data, cluster III comprised a significant number of developmental genes that are involved in the regional specification of leg disc development.…”

DrosophilaImaginal Discs as a Model of Epithelial Wound Repair and Regeneration

“…2E, F). 13 These results are consistent with findings using tissue ablation and irradiation to induce damage. 4,47 This de-specification did not require Wg signaling or regenerative proliferation.…”

“…2 While this method most closely approximates a traumatic wound or amputation, removing the tissue from the animal and subsequently culturing it likely induces additional stress responses. More recently, wounds in the tissue have been induced by pinching through the intact larval cuticle to make a cut 4,11,12 or remove a fragment 13 while leaving the wounded disc in place to heal and regenerate (Fig. 2B).…”

“…(F) After fragmentation, vein and intervein markers are no longer expressed near the wound. 13 JNK, Jun N-terminal kinase; Wg, wingless. To see this illustration in color, the reader is referred to the web version of this article at www.liebertpub.com/wound arrested in G1 or G2.…”

“…To avoid the complications inherent in culturing regenerating tissue, Díaz-García and Baonza have developed a method to cut fragments out of imaginal discs by applying pressure through the larva cuticle. 13 This method leaves the animal intact and enables regeneration to occur in situ. They have observed dramatic changes in cell fate close to the wound edge, as well as at a distance from the wound if the fragment removed is large.…”