Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated.
The mechanisms by which an organism becomes immune competent during its development are largely unknown. When infected by eggs of parasitic wasps, Drosophila larvae mount a complex cellular immune reaction in which specialized host blood cells, lamellocytes and crystal cells, are activated and recruited to build a capsule around the parasite egg to block its development. Here, we report that parasitization by the wasp Leptopilina boulardi leads to a dramatic increase in the number of both lamellocytes and crystal cells in the Drosophila larval lymph gland. Furthermore, a limited burst of mitosis follows shortly after infection, suggesting that both cell division and differentiation of lymph gland hemocytes are required for encapsulation. These changes, observed in the lymph glands of third-instar, but never of second-instar hosts, are almost always accompanied by dispersal of the anterior lobes themselves. To confirm a link between host development and immune competence, we infected mutant hosts in which development is blocked during larval or late larval stages. We found that, in genetic backgrounds where ecdysone levels are low (ecdysoneless) or ecdysone signaling is blocked (nonpupariating allele of the transcription factor broad), the encapsulation response is severely compromised. In the third-instar ecdysoneless hosts, postinfection mitotic amplification in the lymph glands is absent and there is a reduction in crystal cell maturation and postinfection circulating lamellocyte concentration. These results suggest that an ecdysone-activated pathway potentiates precursors of effector cell types to respond to parasitization by proliferation and differentiation. We propose that, by affecting a specific pool of hematopoietic precursors, this pathway thus confers immune capacity to third-instar larvae.
Sorrentino
Richard Paul
RP
Department of Biology, City College of New York and Graduate School and University Center of the City University of New York, 138th Street and Convent Avenue, New York, New York 10031, USA.
Carton
Yves
Y
Govind
Shubha
S
D000818:Animals; D004331:Drosophila melanogaster / Q000196:embryology / Q000276:immunology* / Q000469:parasitology*; D007111:Immunity, Cellular / Q000502:physiology*; D007814:Larva / Q000276:immunology / Q000469:parasitology; D008208:Lymphatic System / Q000276:immunology / Q000469:parasitology; D009154:Mutation; D015398:Signal Transduction / Q000276:immunology; D014863:Wasps / Q000276:immunology*