Phagocytosis in Drosophila: From molecules and cellular machinery to physiology

Melcarne, Claudia; Lemaître, Bruno; Kurant, Estee

doi:10.1016/j.ibmb.2019.04.002

Cited by 72 publications

(81 citation statements)

References 124 publications

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“…Apoptotic cell clearance (efferocytosis) represents another evolutionarily-conserved function performed by embryonic plasmatocytes (Figure 1e; [40]). Therefore, we investigated this function in subpopulations, using numbers of vacuoles per cell as a proxy for this process [18].…”

Section: Resultsmentioning

confidence: 99%

Identification of functionally-distinct macrophage subpopulations regulated by efferocytosis inDrosophila

Brittle

Armitage

et al. 2020

Preprint

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Macrophages are a highly heterogeneous population of cells, with this diversity stemming in part from the existence of tissue resident populations and an ability to adopt a variety of activation states in response to stimuli. Drosophila blood cells (hemocytes) are dominated by a lineage of cells considered to be the functional equivalents of mammalian macrophages (plasmatocytes). Until very recently plasmatocytes were thought to be a homogeneous population. Here, we identify enhancer elements that label subpopulations of plasmatocytes, which vary in abundance across the lifecourse of the fly. We demonstrate that these plasmatocyte subpopulations behave in a functionally-distinct manner when compared to the overall population, including more potent migratory responses to injury and decreased clearance of apoptotic cells within the developing embryo. Additionally, these subpopulations display differential localisation and dynamics in pupae and adults, hinting at the presence of tissue-resident macrophages in the fly. Our enhancer analysis also allows us to identify novel candidate genes involved in plasmatocyte behaviour in vivo. Misexpression of one such enhancer-linked gene (calnexin14D) in all plasmatocytes improves wound responses, causing the overall population to behave more like the subpopulation marked by the calnexin14D-associated enhancer. Finally, we show that, we are able to modulate the number of cells within some subpopulations via exposure to increased levels of apoptotic cell death, thereby decreasing the number of plasmatocytes within more wound-responsive subpopulations. Taken together our data demonstrates the existence of macrophage heterogeneity in Drosophila and identifies mechanisms involved in the specification and function of these plasmatocyte subpopulations. Furthermore, this work identifies key molecular tools with which Drosophila can be used as a highly genetically-tractable, in vivo system to study the biology of macrophage heterogeneity.

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Section: Resultsmentioning

confidence: 99%

Identification of functionally-distinct macrophage subpopulations regulated by efferocytosis inDrosophila

Brittle

Armitage

et al. 2020

Preprint

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“…The scavenger receptors and the opsonins cover a large panel of pathogens (For review see (Melcarne et al, 2019)), indicating an overall switch for hemocytes function from apoptotic body scavenging and cuticle production at embryonic stages to pathogen scavenging at the WL stage. Since it was previously shown that the hemocytes present in the embryo are able of phagocytosis (Tan et al, 2014; Vlisidou et al, 2009), we compared the phagocytic capacity of hemocytes from E16 and WL and exposed them to fluorescent beads.…”

Section: Resultsmentioning

confidence: 99%

Temporal specificity and heterogeneity of the fly immune cells’ transcriptional landscape

Cattenoz

Sakr

Pavlidaki

et al. 2019

Preprint

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Summary Immune cells provide defense against the non-self, however recent data suggest roles well beyond innate immunity, in processes as diverse as development, metabolism and tumor progression. Nevertheless, the heterogeneity of these cells remains an open question. Using bulk RNA sequencing we find that the Drosophila immune cells (hemocytes) display distinct features in the embryo, a closed and rapidly developing system, compared to the larva, which is exposed to environmental and metabolic challenges. Through single cell RNA sequencing we identify fourteen hemocyte clusters present in unchallenged larvae and associated with distinct cellular processes e.g. proliferation, phagocytosis, metabolic homeostasis and humoral response. Finally, we characterize the changes occurring in the hemocyte clusters upon wasp infestation that triggers the differentiation of a novel cell type, the lamellocyte. This first molecular atlas provides precious insights and paves the way to study the biology of the Drosophila immune cells in physiological and pathological conditions.

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“…Both Scavenger receptors and integrins are known to act as membrane receptors in phagocytosis of bacteria and apoptotic cells (77). In addition, integrins are involved in diverse processes, including cell motility and adhesion, and encapsulation (78, 79). The hemolin is known to act as an opsonin by increasing phagocytosis and nodulation of bacteria in Manduca sexta (80).…”

Section: Resultsmentioning

confidence: 99%

“…They encoded 2 Rho GTPase Activating Proteins (RhoGAP-like), a scavenger receptor similar to the D. melanogaster Croquemort receptor (SR-B3) and a homolog of the D. melanogaster integrin α-PS1. In D. melanogaster , Croquemort has been shown to take part in phagocytosis of apoptotic cells and of the Gram positive bacterium Staphylococcus aureus but not of the Gram negative bacterium Escherichia coli (79, 86). Integrin α-PS1 is a ligand of the extracellular matrix protein laminin (87).…”

Section: Resultsmentioning

confidence: 99%

Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

Huot

Bigourdan

Pagès

et al. 2019

Preprint

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13The Steinernema carpocapsae-Xenorhabdus nematophila association is a nematobacterial complex (NBC) 14 used in biological control of insect crop pests. The ability of this dual pathogen to infest and kill an insect 15 strongly depends on the dialogue between the host's immune system and each partner of the complex. Even 16 though this dialogue has been extensively studied from the two partners' points of view in several insect 17 models, still little is known about the structure and the molecular aspects of the insects' immune response 18 to the dual infection. Here, we used the lepidopteran pest Spodoptera frugiperda as a model to analyze the 19 respective impact of each NBC partner in the spatiotemporal immune responses that are induced after 20 infestation. To this aim, we first analyzed the expression variations of the insect's immune genes in the fat 21 bodies and hemocytes of infested larvae by using previously obtained RNAseq data. We then selected 22 representative immune genes for RT-qPCR investigations of the temporal variations of their expressions 23 after infestation and of their induction levels after independent injections of each partner. We found that 24 the fat body and the hemocytes both produce potent and stable immune responses to the infestation by the 25 NBC, which correspond to combinations of bacterium-and nematode-induced ones. Consistent with the 26 nature of each pathogen, we showed that X. nematophila mainly induces genes classically involved in 27 antibacterial responses, whereas S. carpocapsae is responsible for the induction of lectins and of genes 28 expected to be involved in melanization and cellular encapsulation. In addition, we found that two clusters 29 of unknown genes dramatically induced by the NBC also present partner-specific induction profiles, which 30 paves the way for their functional characterization. Finally, we discuss putative relationships between the 31 variations of the expression of some immune genes and the NBC's immunosuppressive strategies. 32 3 33Author summary 34 Entomopathogenic nematodes (EPNs) are living in the soil and prey upon insect larvae. They enter the 35 insect by the natural orifices, and reach the hemocoel through the intestinal epithelium. There, they release 36 their symbiotic bacteria that will develop within the insect and eventually kill it. Nematodes can then feed 37 and reproduce on the insect cadaver. By using transcriptomic approaches, we previously showed that 38 Lepidoptera larvae (caterpillars of the fall armyworm Spodoptera frugiperda) produce a strong immune 39 response in reaction to infestation by EPNs. However, we do not know if this immune reaction is triggered 40 by the nematode itself -Steinernema carpacapsae -or its symbiotic bacteria -Xenorhabdus nematophila. 41 To answer this question, we present in this work a careful annotation of immunity genes in S. frugiperda 42 and surveyed their activation by quantitative PCR in reaction to an injection of the bacteria alone, the axenic 43 nematode or the ...

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Phagocytosis in Drosophila: From molecules and cellular machinery to physiology

Cited by 72 publications

References 124 publications

Identification of functionally-distinct macrophage subpopulations regulated by efferocytosis inDrosophila

Identification of functionally-distinct macrophage subpopulations regulated by efferocytosis inDrosophila

Temporal specificity and heterogeneity of the fly immune cells’ transcriptional landscape

Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

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