Drosophila embryonic pattern repair: how embryos respond to cyclin E-induced ectopic division.

The Drosophila melanogaster embryo ordinarily undergoes thirteen cycles of rapid syncytial division followed by three rounds of cellular division for most cells. Strict regulation of the number of divisions is believed to be essential for normal patterning and development. To determine how the embryo responds to hyperplastic growth, we have examined epidermal development in embryos that experience additional rounds of mitosis as the result of ectopic Cyclin E expression. We observed that the cell density in the epidermis nearly doubled within 1 hour of Cyclin E induction. The spacing and width of the ENGRAILED and wingless stripes was unchanged, but the cell density within the stripes was increased. By 4 hours after Cyclin E induction, the cell density had returned to almost normal values. The embryos developed, albeit more slowly, to produce viable larvae and adults. The excess cells were removed by apoptosis in a reaper-dependent fashion as evidenced by increased reaper expression. Embryos lacking cell death in the abdomen exhibited changes in ENGRAILED expression. In addition, germband retraction and dorsal closure were slower than normal. Ectopic Cyclin E expression in cell-death-deficient embryos exacerbated the germband retraction and ENGRAILED-expression defects.

Patterned epidermal cell death in wild-type and segment polarity mutant Drosophila embryos.

Programmed cell death plays an essential role in the normal embryonic development of Drosophila melanogaster. One region of the embryo where cell death occurs, but has not been studied in detail, is the abdominal epidermis. Because cell death is a fleeting process, we have used time-lapse, fluorescence microscopy to map epidermal apoptosis throughout embryonic development. Cell death occurs in a stereotypically striped pattern near both sides of the segment border and to a lesser extent in the middle of the segment. This map of wild-type cell death was used to determine how cell death patterns change in response to genetic perturbations that affect epidermal patterning. Previous studies have suggested that segment polarity mutant phenotypes are partially the result of increased cell death. Mutations in wingless, armadillo, and gooseberry led to dramatic increases in apoptosis in the anterior of the segment while a naked mutation resulted in a dramatic increase in the death of engrailed cells in the posterior of the segment. These results show that segment polarity gene expression is necessary for the survival of specific rows of epidermal cells and may provide insight into the establishment of the wild-type epidermal cell death pattern.

Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration.

The product of the maternal effect gene, bicoid (bcd), is a transcription factor that acts in a concentration-dependent fashion to direct the establishment of anterior fates in the Drosophila melanogaster embryo. Embryos laid by mothers with fewer or greater than the normal two copies of bcd show initial alterations in the expression of the gap, segmentation and segment polarity genes, as well as changes in early morphological markers. In the absence of a fate map repair system, one would predict that these initial changes would result in drastic changes in the shape and size of larval and adult structures. However, these embryos develop into relatively normal larvae and adults. This indicates that there is plasticity in Drosophila embryonic development along the anterior-posterior axis. Embryos laid by mothers with six copies of bcd have reduced viability, indicating a threshold for repairing anterior-posterior mispatterning. We show that cell death plays a major role in correcting expanded regions of the fate map. There is a concomitant decrease of cell death in compressed regions of the fate map. We also show that compression of the fate map does not appear to be repaired by the induction of new cell divisions. In addition, some tissues are more sensitive to fate map compression than others.