Implication of the linotte (lio) gene in Drosophila brain development

A. SIMON (P), M. SYNGUELAKIS, T. PREAT

  Institut Alfred Fessard, 91190 Gif-sur-Yvette, France,

Linotte (lio) has been screened as a memory mutant (1). The lio gene encodes a putative transmembrane receptor of the tyrosine protein kinase family, homologous to the human RYK gene product (2). These proteins are unique among receptor tyrosine kinases, since they possess a short extracellular domain and a modified intracellular catalytic domain. Independently, the same gene was cloned -and named derailed- by the group of J.B. Thomas, after a screen for axonal guidance defects in embryonic peripherial nervous systeme (3). We show that a deletion of the lio gene causes structural defects in the central part of the adult brain. Both the central complex and the mushroom bodies are affected. Recent results from Moreau and Dura show a developmental rescue of the lio defect with constructions carrying the lio gene (cf accompaying abstract). These results suggest that the lio kinase is part of a novel signal transduction cascade involved in the brain development.
We generated an antibody which allowed us to reveal the expression of the lio protein in the nervous system at different stages of development. In the larvae, the expression in the brain is restricted to the optic ganglion primordium and in four neurons at the junction of the two cerebral hemispheres. We think that lio gene expression in these four neurons is necessary for the correct development of a central part of the adult brain. For the moment, we want to understand how the absence of expression in the four interhemispheric cells in the larvae could lead to such an important and complex defect in the adult. When the lio gene is absent, there is either a quantitative cell defect (abnormal proliferation of neuroblasts or cell death), or an axonal guidance defect. To distinguish among these possibilities, specific markers were expressed in these four interhemispheric cells in a mutant context. Thus, we dissected the regulatory domains controlling the lio gene expression. Several genomic DNA fragments have been subcloned upstream of the reporter gene lacZ, in a transposable P element. A 1,3 kb fragment leads to specific expression in the interhemispheric larval cells. This construction allowed us to show that these cells are still present in animals deleted for the lio gene. We are currently using a diffusible marker to follow the axons in a mutant context. Our working hypothesis is that the four pioneer neurons would serve as guides for the differentiation, during metamorphosis of specific central brain structures.
We are using Gal4 lines obtained in the laboratory after P-element mutagenesis to observe more precisely how central brain structures are affected in lio mutants. Finally, we will put the lio gene downstream of the 1,3 kb regulatory sequence to test if lio expression in these four cells is sufficient to rescue both the structural and behavioral phenotypes.

References:

(1): Dura J.M., Preat T. and Tully T. (1993) J. Neurogenet. 9, 1-14. (2): Dura J.M., Taillebourg E. and Preat T. (1995) FEBS letters 370, 250-254. (3): Callahan C.A., Muralidhar M.G., Lundgren S.E., Scully A.L., Thomas J.B. (1995) Nature 376, 171-174.