To investigate the molecular mechanisms responsible for the temporal and spatial control of cell movements

During embryonic development of multicellular organisms, a variety of cell types undergo temporally and spatially controlled cell migrations. Although cell motility is believed to involve dynamic changes in cell adhesion and rearrangement of the cytoskeleton, the molecular mechanisms regulating these activities are not well understood. In addition, the factors controlling the coordination of migratory behavior with cell fate determination and differentiation during embryonic development remain to be elucidated. Transcription factors would be expected to play a major role in these events and several transcription factors have been shown to be required for specific cell movements during development (Montell et al., 1992; Salser and Kenyon, 1992; Miller et al., 1992; Garriga et al., 1993; Klambt et al., 1993; Anderson, 1995). However the downstream targets mediating these effects are not known. We have been studying the migration of 6-10 follicle cells, known as the border cells, in the Drosophila ovary as a model system to address these questions. Egg chambers in the ovary comprise a cluster of sixteen germline cells (fifteen nurse cells and 1 oocyte) surrounded by a monolayer epithelium of somatic follicle cells (Fig. 1). During stage 9 of oogenesis (see Spradling, 1993, for review of oogenesis), the majority of the 1100 follicle cells begin a posteriorward displacement so that eventually more than 95% will stack up to form a columnar epithelium in contact with the oocyte (Fig. 1). Of the remaining 5%, most will stretch to cover the large nurse cell cluster. However a group of 6-10 cells remains rounded at the anterior tip of the egg chamber until mid stage 9 (Fig. 1) when they extend processes in between the nurse cells and migrate through the nurse cell cluster to the oocyte border. These so-called border cells serve at least 2 essential functions in oogenesis: they participate in formation of the eggshell structure known as the micropyle, maintaining an opening through which the sperm enters at fertilization (Montell et al., 1992); and they secrete the Torso-like protein, which is an essential patterning signal (Savant-Bhonsale and Montell, 1993). Previously we have shown that initiation of border cell migration is controlled by the slow border cells (slbo) locus (Montell et al., 1992). Weak slbo mutations cause delayed border cell migration whereas stronger alleles result in complete failure of migration (Montell, 1992; Fig. 1) causing female sterility; null mutations are embryonic lethal. The slbo locus encodes the Drosophila homolog of C/EBP, a basic region/leucine zipper transcription factor. In vertebrates C/EBPα is a terminal differentiation factor required for expression of cell-type specific products (Friedman et al., 1989; Christy et al., 1989; Lin and Lane, 1992; Umek et al., 1991). Drosophila C/EBP has been shown to be a DNA binding protein (Rørth and Montell, 1992) and a transcriptional activator in vitro (Rørth, 1994). Therefore to elucidate the 2255 Development 121, 2255-2263 (1995) Printed in Great Britain © The Company of Biologists Limited 1995