Reactive oxygen species-dependent Toll/NF-κB activation in the Drosophila hematopoietic niche confers resistance to wasp parasitism

Louradour, Isabelle; Sharma, Anurag; Morin-Poulard, Ismaël; Letourneau, Manon; Víncent, Alaín; Crozatier, Michèle; Vanzo, Nathalie

doi:10.7554/elife.25496

Cited by 86 publications

(114 citation statements)

References 75 publications

(131 reference statements)

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“…Besides, AP fate is controlled by systemic cues and external stresses such as immune challenge (Krzemien et al, 2010, Khadilkar et al, 2017b. In particular, deposition of egg from the parasitoid wasp Leptopilina boulardi (L. boulardi) in the hemocoel triggers AP differentiation into lamellocytes and premature histolysis of the primary lobes (Lanot et al, 2001, Crozatier et al, 2004, Louradour et al, 2017, Benmimoun et al, 2015, Bazzi et al, 2018, Letourneau et al, 2016, Small et al, 2014. ROS-mediated activation of EGFR and Toll/NF-kB signaling pathways in the PSC and the consecutive down-regulation of the JAK-STAT pathway in the AP are essential for this cellular immune response (Makki et al, 2010, Louradour et al, 2017.…”

Section: Introductionmentioning

confidence: 99%

Differential activation of JAK-STAT signaling in blood cell progenitors reveals functional compartmentalization of theDrosophilalymph gland

Rodrigues

Renaud

VijayRaghavan

et al. 2020

Preprint

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Blood cells arise from diverse pools of stem and progenitor cells. Understanding progenitor heterogeneity is a major challenge. The Drosophila larval lymph gland is a well-studied model to understand blood progenitor maintenance and recapitulates several aspects of vertebrate hematopoiesis. However in-depth analysis has focused on progenitors located in lymph gland anterior lobes (AP), ignoring the progenitors from the posterior lobes (PP). Using in situ expression mapping and transcriptome analysis we reveal PP heterogeneity and identify molecular-genetic tools to study this abundant progenitor population. Functional analysis shows that PP resist differentiation upon immune challenge, in a JAK-STAT-dependent manner. Upon wasp parasitism, AP downregulate JAK-STAT signaling and form lamellocytes. In contrast, we show that PP activate STAT92E and remain undifferentiated. Stat92E knockdown in PP or genetically reducing JAK-STAT signaling permits PP lamellocyte differentiation. We discuss how heterogeneity and compartmentalization allow functional segregation in response to systemic cues and could be widely applicable.HighlightsWe provide an in situ and transcriptome map of larval blood progenitors Posterior lymph gland progenitors are refractory to immune challenge STAT activation after wasp parasitism maintains posterior progenitors

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Section: Introductionmentioning

confidence: 99%

Differential activation of JAK-STAT signaling in blood cell progenitors reveals functional compartmentalization of theDrosophilalymph gland

Rodrigues

Renaud

VijayRaghavan

et al. 2020

Preprint

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“…The second hemocyte lineage derives from the lymph gland, a specialized organ that develops along all larval stages. The lymph gland acts as a reservoir of both prohemocytes and mature hemocytes, which are released at the onset of metamorphosis or upon parasitization [8], [14]- [17]. Both blood cell lineages persist into the adult stage of the fly [18].…”

Section: Introductionmentioning

confidence: 99%

Two Nimrod receptors, NimC1 and Eater, synergistically contribute to bacterial phagocytosis inDrosophila melanogaster

Melcarne

Ramond

Dudzic

et al. 2018

Preprint

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Eater and NimC1 are transmembrane receptors of the Drosophila Nimrod family, specifically expressed in hemocytes, the insect blood cells. Previous ex vivo and in vivo RNAi studies have pointed to their role in the phagocytosis of bacteria. Here, we have created a novel null mutant in NimC1 to re-evaluate the role of NimC1, alone or in combination with Eater, in the cellular immune response. We show that NimC1 functions as an adhesion molecule ex vivo, but in contrast to Eater is not required for hemocyte sessility in vivo. Ex vivo phagocytosis assays and electron microscopy experiments confirmed that Eater is the main phagocytic receptor for

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“…The second haemocyte lineage derives from the lymph gland, a specialized organ that develops along all larval stages. The lymph gland acts as a reservoir of both prohaemocytes and mature haemocytes, which are released at the onset of metamorphosis or upon parasitization [8,[27][28][29][30]. Finally, accumulating evidence suggests that the sessile haematopoietic pockets also function as an active peripheral haematopoietic niche [21,23,26].…”

Section: Nimc1 Null Larvae Have An Increased Number Of Haemocytesmentioning

confidence: 99%

Two Nimrod receptors, NimC1 and Eater, synergistically contribute to bacterial phagocytosis in Drosophila melanogaster

et al. 2019

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Eater and NimC1 are transmembrane receptors of the Drosophila Nimrod family, specifically expressed in haemocytes, the insect blood cells. Previous ex vivo and in vivoRNAi studies have pointed to their role in the phagocytosis of bacteria. Here, we have created a novel NimC1 null mutant to re‐evaluate the role of NimC1, alone or in combination with Eater, in the cellular immune response. We show that NimC1 functions as an adhesion molecule ex vivo, but in contrast to Eater it is not required for haemocyte sessility in vivo. Ex vivo phagocytosis assays and electron microscopy experiments confirmed that Eater is the main phagocytic receptor for Gram‐positive, but not Gram‐negative bacteria, and contributes to microbe tethering to haemocytes. Surprisingly, NimC1 deletion did not impair phagocytosis of bacteria, nor their adhesion to the haemocytes. However, phagocytosis of both types of bacteria was almost abolished in NimC11;eater1 haemocytes. This indicates that both receptors contribute synergistically to the phagocytosis of bacteria, but that Eater can bypass the requirement for NimC1. Finally, we uncovered that NimC1, but not Eater, is essential for uptake of latex beads and zymosan particles. We conclude that Eater and NimC1 are the two main receptors for phagocytosis of bacteria in Drosophila, and that each receptor likely plays distinct roles in microbial uptake.

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Reactive oxygen species-dependent Toll/NF-κB activation in the Drosophila hematopoietic niche confers resistance to wasp parasitism

Cited by 86 publications

References 75 publications

Differential activation of JAK-STAT signaling in blood cell progenitors reveals functional compartmentalization of theDrosophilalymph gland

Differential activation of JAK-STAT signaling in blood cell progenitors reveals functional compartmentalization of theDrosophilalymph gland

Two Nimrod receptors, NimC1 and Eater, synergistically contribute to bacterial phagocytosis inDrosophila melanogaster

Two Nimrod receptors, NimC1 and Eater, synergistically contribute to bacterial phagocytosis in Drosophila melanogaster

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