Abstract
Drosophila immune response involves three types of hemocytes (‘blood cells’). One cell type, the lamellocyte, is induced to differentiate only under particular conditions, such as parasitization by wasps. Here, we have investigated the mechanisms underlying the specification of lamellocytes. We first show that collier (col), the Drosophila orthologue of the vertebrate gene encoding early B-cell factor (EBF), is expressed very early during ontogeny of the lymph gland, the larval hematopoietic organ. In this organ, Col expression prefigures a specific posterior region recently proposed to act as a signalling centre, the posterior signalling centre (PSC). The complete lack of lamellocytes in parasitized col mutant larvae revealed the critical requirement for Col activity in specification of this cell type. In wild-type larvae, Col expression remains restricted to the PSC following parasitization, despite the massive production of lamellocytes. We therefore propose that Col endows PSC cells with the capacity to relay an instructive signal that orients hematopoietic precursors towards the lamellocyte fate in response to parasitization. Considered together with the role of EBF in lymphopoiesis, these findings suggest new parallels in cellular immunity between Drosophila and vertebrates. Further investigations on Col/EBF expression and function in other phyla should provide fresh insight into the evolutionary origin of lymphoid cells.
Highlights
Hematopoiesis in Drosophila shares several features with the analogous process in vertebrates
Striking similarities with vertebrate hematopoiesis were revealed when it was shown that Serpent (Srp), a GATA factor, and Lozenge (Lz), a transcription factor related to Runx1/AML1, are required for the development of hemocytes and of crystal cells, respectively (Rehorn et al 1996; Lebestky et al 2000; Orkin 2000)
Our data show that (i) Col expression defines a specific group of cells within the lymph glands; (ii) lamellocyte differentiation, which is an exclusive feature of lymph gland hematopoiesis, depends upon Col activity; and (iii) the massive production of lamellocytes that follows parasitization does not involve changes in Col expression
Summary
Hematopoiesis in Drosophila shares several features with the analogous process in vertebrates. We observed that Col is expressed in two discrete clusters of cells in the dorsal mesoderm of thoracic segments T2 and T3, starting at the germ-band extension, when lymph gland hemocyte precursors become specified (stage 11; Figure 1A) (Holz et al 2003). In lymph gland precursors prior to stage 12 (Berkeley Drosophila Genome Project gene expression report [http:// www.fruitfly.org/cgi-bin/ex/insitu.pl]; Lebestky et al 2003) Consistent with this result, larval hematopoietic progenitors expressing Col are observed in srp6G (an amorphic allele; Rehorn et al 1996) mutant embryos (Figure 1I), indicating that the specification of the embryonic and larval lymph gland progenitors may involve different processes. Numerous crystal cells differentiate in col mutant lymph glands, including in secondary lobes, despite the loss of Ser expression in the PSC (see Figures 4E, 4F, 5A, and 5B). The absence of lamellocytes after parasitization that is associated with the increase in the number of crystal cells in col mutant lymph glands, and the opposite situation in srpDGal4/UAS-col lymph glands (Figure 5; Table 1), support the existence of bipotential crystal cell/lamellocyte precursors
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