Neuron-glia interactions in the nervous system of Drosophila embryos

Abstract

Several cell lineages derived from the mesectoderm occupy and contact axons in the midline of the developing Drosophila CNS. Which of these midline cell lineages contribute to commissural axon morphogenesis? In the absence of the midline cells as in mutant embryos of the single-minded gene, the longitudinal axons collapse at the midline and commissural axons are absent. Despite the similarity in axon tract phenotype, the midline cells in slit mutant embryos survive but are displaced. Correct cytoarchitecture of the midline cells is therefore dependent on the activity of Sli protein which is in turn necessary for commissure formation. In mutant embryos displaying a fused commissure phenotype (rhomboid and Star), the anterior and middle midline glia cells failed to migrate and died by apoptosis after commissure development. In these mutants the number of cells in midline neuronal lineages was reduced before defects in midline glia were apparent. In wildtype embryos approximately 50% of cells in three midline glia lineages died by apoptosis after commissure separation as shown by ultrastructural and enhancer trap analysis. Midline glia lineages died by apoptosis as shown morphologically and by their survival in embryos deficient in the cell death gene reaper. Quantitative analysis revealed variable survival of cells in the anterior, middle and posterior midline glial lineages during embryogenesis suggesting heterogeneity among these cells. The presence of extra anterior, middle and posterior midline glial lineages relative to wildtype numbers in reaper mutant embryos suggested that cell death regulates either midline glial proliferation or cell fate determination during wildtype embryogenesis. Alterations in axon-glia contact correlated with changes in midline glia survival. What happens to apoptotic cells in the Drosophila embryonic central nervous system? A variety of glia in the nervous system were capable of phagocytic activity including midline glia, longitudinal tract glia, nerve root glia and subperineurial glia, revealed by electron microscopy. However, the majority of apoptotic cells in the central nervous system were engulfed by subperineurial glia. In the absence of phagocytic haemocytes in embryos mutant for the Bicaudal-d gene, most apoptotic cells were retained in subperineurial glia at the outer edges of the central nervous system. Apoptotic cells were expelled from the central nervous system of Bicaudal-d mutant embryos suggesting that phagocytic haemocytes participate in the removal of apoptotic cells from the central nervous system but are not essential for this process.