Cellular Immune Response to Parasite Infection in the Drosophila Lymph Gland Is Developmentally Regulated

Abstract

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.

Cell lineage tracing reveals the plasticity of the hemocyte lineages and of the hematopoietic compartments in Drosophila melanogaster

“…Our knowledge regarding these cells is fragmentary, and further studies are required to explore their possible function in metamorphosis and in adult life. It was earlier shown that lamellocytes originate from the sessile hematopoietic compartment , and also from the lymph gland (Sorrentino et al, 2002).…”

Structural and functional characterization of pseudopodocyte, a shaggy immune cell produced by two Drosophila species of the obscura group

“…They are considered essential for encapsulation and were long described as a plasmatocyte-derived form Rizki, 1980, 1984). Many studies established that plasmatocytes and lamellocytes follow specific differentiation pathways (Lanot et al, 2001;Sorrentino et al, 2002Sorrentino et al, , 2004Meister, 2004;Crozatier et al, 2004;Krzemień et al, 2007). However, recent works on Drosophila hemocytes lineage showed that plasmatocytes could indeed differentiate into lamellocytes (Honti et al, 2010;Avet-Rochex et al, 2010;Stofanko et al, 2010).…”

Fluorescence-activated cell sorting (FACS) of Drosophila hemocytes reveals important functional similarities to mammalian leukocytes

“…Whole-animal functional studies have suggested that Drosophila hemocytes participate in similar activities to mammalian leukocytes, including phagocytosis͞encapsulation of pathogens, release of reactive oxygen species (ROS) and reactive nitrogen species and antimicrobial peptides, activation of humoral serine protease cascades, scavenging of dead bodies, wound repair, and extracellular matrix deposition (1)(2)(3)(4)(5)(6). Molecular genetic studies have unravelled important evolutionarily conserved regulatory elements, including transcription factors of the Runt͞acute myelogenous leukemia (7), GATA (8), and Polycomb (9) families and integral transduction cascades, including the immune deficiency͞tumor necrosis receptor (2), Toll͞IL-1 receptor (2), Janus kinase (10,11), mitogen-activated protein kinase (12), Notch (13), steroid (14), and vascular endothelial growth factor (15) pathways.…”