Regulation and metamorphosis of the abdominal histoblasts ofDrosophila melanogaster

Abstract

The development of the adult abdomen ofDrosophila melanogaster was analyzed by histology, microcautery, and genetic strategies. Eight nests of diploid histoblasts were identified in the newly hatched larva among the polytene epidermal cells of each abdominal segment: pairs of anterior dorsal, posterior dorsal, and ventral histoblast nests and a pair of spiracular anlagen. The histoblasts do not divide during larval life but begin dividing rapidly 3 h after pupariation, doubling every 3.6 h. Initially they remain confined to their original area, but 15 h after pupariation the nests enlarge, and histoblasts replace adjacent epidermis cell by cell. The histoblasts cover half the abdomen by 28 h after pupariation and the rest by 36 h. Polytene epidermal cells of the intersegmental margin are replaced last. Cautery of the anterior dorsal nest caused deletion of the whole corresponding hemitergite, whereas cautery of the posterior dorsal nest caused the deletion of the macrochaetae of the posterior of the hemitergite. Cautery of the ventral nest deleted the hemisternite and the pleura, whereas cautery of the spiracular anlagen deleted the spiracle. Results of cautery also revealed that no macrochaetae formed on the tergite in the absence of adjacent microchaetae. Clonal analysis revealed that there were no clonal restrictions within a hemitergite at pupariation. Cautery of polytene epidermal cells other than those of the intersegmental margin failed to affect tergite development. However, cautery of polytene epidermal cells of the intersegmental margin adjacent to either dorsal histoblast nest caused mirror-image duplications of the anterior or posterior of the hemitergite in 10% of the hemitergites. Forty percent of the damaged presumptive hemitergites formed complete hemitergites, indicating extensive pattern regulation and regeneration. Pattern duplication and regeneration were accounted for in terms of intercalation and a model of epimorphic pattern regulation (French et al., 1976). Histoblasts in adjacent segments normally develop independently, but if they are enabled to interact by deleting the polytene epidermal cells of the intersegmental margin, they undergo intercalation which results in duplication or regeneration. The possible role of the intersegmental margin cells of insects in development was analyzed.

Integrating transcription kinetics with alternative polyadenylation and cell cycle control

“…Higher insects, i.e., those that undergo a complete metamorphosis, possess imaginal cells, a particular group of tissue-specific stem cell-like progenitors having unique characteristics, 30 and from which different adult structures originate during pupariation. The precursors of the adult abdomen epidermis are called abdominal histoblasts, 31 small cells specified during embryogenesis that show a characteristic pattern of cell cycle divisions: they arrest at the G 2 phase of mitosis but continue to grow in size throughout the larval instars until the onset of metamorphosis. At this stage they go through very rapid cell cycles and start to proliferate, showing the highest proliferation rate among all the imaginal cells during pupariation.…”

“…At this stage they go through very rapid cell cycles and start to proliferate, showing the highest proliferation rate among all the imaginal cells during pupariation. [31][32][33] As a result, they expand and displace the surrounding larval epithelial cells (LECs) to form the abdominal epidermis. 32,34 When the abdominal histoblasts of the DpA2 transgenic individuals were analyzed by microscopy, we observed that they failed to proliferate at the pupa stage.…”

Extrinsic and intrinsic mechanisms directing epithelial cell sheet replacement duringDrosophilametamorphosis

“…Each anterior dorsal and ventral nest is composed of approximately 16 cells; each posterior dorsal nest consists of approximately five cells; and each spiracle nest has approximately three cells (Fig. 1A) (Guerra et al, 1973;Roseland and Schneiderman, 1979;Madhavan and Madhavan, 1980). During larval stages histoblasts are mitotically quiescent and arrested in G2 (Garcia-Bellido and Merriam, 1971;Madhavan and Schneiderman, 1977;Roseland and Schneiderman, 1979).…”

“…1A) (Guerra et al, 1973;Roseland and Schneiderman, 1979;Madhavan and Madhavan, 1980). During larval stages histoblasts are mitotically quiescent and arrested in G2 (Garcia-Bellido and Merriam, 1971;Madhavan and Schneiderman, 1977;Roseland and Schneiderman, 1979). At the onset of metamorphosis histoblasts undertake a rapid proliferation that allows them to expand and fuse, at the expense of the preexisting surrounding polyploid larval epidermal cells (LECs) that commit programmed cell death (Madhavan and Madhavan, 1980).…”

Cell rearrangements, cell divisions and cell death in a migrating epithelial sheet in the abdomen ofDrosophila

“…The histoblasts divide and migrate dorsally and ventrally over the abdomen until its whole surface is covered with cells (Madhavan and Madhavan, 1980;Ninov et al, 2007;Roseland and Schneiderman, 1979). During this process, the LECs undergo apoptosis; they constrict apically, are extruded from the epithelium and are subsequently phagocytosed by hemocytes, which patrol underneath the epithelium (Ninov et al, 2007).…”