The vascular niche controls Drosophila hematopoiesis via fibroblast growth factor signaling

Destalminil-Letourneau, Manon; Morin-Poulard, Ismaël; Tian, Yan; Vanzo, Nathalie; Crozatier, Michèle

doi:10.7554/elife.64672

Cited by 27 publications

(30 citation statements)

References 62 publications

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“…Sar1 regulates the formation of coat protein complex II (COPII), which is involved in transporting the newly synthesized proteins from the endoplasmic reticulum to the Golgi [ 56 – 58 ]. Downregulating sar1 , thus, leads to the intracellular accumulation of proteins that are otherwise meant to be released extracellularly [ 59 , 60 ]. Downregulation of sar1 function by Kn 13A11 -Gal4 following the scheme ( S6A Fig ) resulted in a drastic increase in differentiation and overall size of the lymph gland ( S6B–S6C′ Fig , and quantitated in S6E–S6G Fig ).…”

Section: Resultsmentioning

confidence: 99%

“…The multi-lobed lymph gland that spans from thoracic to abdominal segment with its stockpile of progenitors at different developmental stages provides us with a unique opportunity to unravel signals dedicated to their maintenance. The extrinsic, intrinsic, and systemic signals critical for maintaining the primary lobe progenitors have been extensively worked out [ 2 , 16 , 59 ]. In comparison, our understanding of the cells in the posterior lobe is limited.…”

Section: Discussionmentioning

confidence: 99%

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Ubx-Collier signaling cascade maintains blood progenitors in the posterior lobes of the Drosophila larval lymph gland

et al. 2021

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Drosophila larval hematopoiesis occurs in a specialized multi-lobed organ called the lymph gland. Extensive characterization of the organ has provided mechanistic insights into events related to developmental hematopoiesis. Spanning from the thoracic to the abdominal segment of the larvae, this organ comprises a pair of primary, secondary, and tertiary lobes. Much of our understanding arises from the studies on the primary lobe, while the secondary and tertiary lobes have remained mostly unexplored. Previous studies have inferred that these lobes are composed of progenitors that differentiate during pupation; however, the mechanistic basis of this extended progenitor state remains unclear. This study shows that posterior lobe progenitors are maintained by a local signaling center defined by Ubx and Collier in the tertiary lobe. This Ubx zone in the tertiary lobe shares several markers with the niche of the primary lobe. Ubx domain regulates the homeostasis of the posterior lobe progenitors in normal development and an immune-challenged scenario. Our study establishes the lymph gland as a model to tease out how the progenitors interface with the dual niches within an organ during development and disorders.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Ubx-Collier signaling cascade maintains blood progenitors in the posterior lobes of the Drosophila larval lymph gland

et al. 2021

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“…Altogether, these data indicate that through the activation of Fibroblast Growth Factor (FGF) signaling, the vascular system prevents hematopoietic progenitors from massive differentiation, ensuring the proper balance between blood cell populations within the lymph gland. For the first time, this study provides evidence that the vascular system, which directly controls blood cell progenitors independently from the PSC, acts as a niche [Figure 2B and (84)]. In conclusion, two distinct niches, the PSC and the cardiac tube, control lymph gland homeostasis.…”

Section: The Cardiac Tube Functions As a Hematopoietic Nichementioning

confidence: 72%

Drosophila as a Model to Study Cellular Communication Between the Hematopoietic Niche and Blood Progenitors Under Homeostatic Conditions and in Response to an Immune Stress

2021

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In adult mammals, blood cells are formed from hematopoietic stem progenitor cells, which are controlled by a complex cellular microenvironment called “niche”. Drosophila melanogaster is a powerful model organism to decipher the mechanisms controlling hematopoiesis, due both to its limited number of blood cell lineages and to the conservation of genes and signaling pathways throughout bilaterian evolution. Insect blood cells or hemocytes are similar to the mammalian myeloid lineage that ensures innate immunity functions. Like in vertebrates, two waves of hematopoiesis occur in Drosophila. The first wave takes place during embryogenesis. The second wave occurs at larval stages, where two distinct hematopoietic sites are identified: subcuticular hematopoietic pockets and a specialized hematopoietic organ called the lymph gland. In both sites, hematopoiesis is regulated by distinct niches. In hematopoietic pockets, sensory neurons of the peripheral nervous system provide a microenvironment that promotes embryonic hemocyte expansion and differentiation. In the lymph gland blood cells are produced from hematopoietic progenitors. A small cluster of cells called Posterior Signaling Centre (PSC) and the vascular system, along which the lymph gland develops, act collectively as a niche, under homeostatic conditions, to control the balance between maintenance and differentiation of lymph gland progenitors. In response to an immune stress such as wasp parasitism, lymph gland hematopoiesis is drastically modified and shifts towards emergency hematopoiesis, leading to increased progenitor proliferation and their differentiation into lamellocyte, a specific blood cell type which will neutralize the parasite. The PSC is essential to control this emergency response. In this review, we summarize Drosophila cellular and molecular mechanisms involved in the communication between the niche and hematopoietic progenitors, both under homeostatic and stress conditions. Finally, we discuss similarities between mechanisms by which niches regulate hematopoietic stem/progenitor cells in Drosophila and mammals.

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“…Immune assaults and environmental challenges accelerate the differentiation of lymph gland progenitors and the release of differentiated plasmatocytes and other immune cells into circulation (Sorrentino et al, 2002;Crozatier et al, 2004;Márkus et al, 2005;Owusu-Ansah and Banerjee, 2009;Shim et al, 2013;Letourneau et al, 2016;Banerjee et al, 2019). Likewise, dysregulation of various major signaling pathways that usually tightly control normal lymph gland development can result in premature, or precocious, differentiation, including signaling by Notch (N), Hedgehog (Hh), Wingless (Wg), the Bone Morphogenetic Protein (BMP) Decapentaplegic (Dpp), receptor tyrosine kinases such as the PDGFR/VEGFR-related Receptor (PVR) and Fibroblast Growth Factor Receptor (FGFR), Hippo, JAK/STAT, NFκB-related Toll signaling and transcriptional regulators such as the zinc finger transcription factor Zfrp8 and the GATA factor Pannier (Qiu et al, 1998;Myrick and Dearolf, 2000;Lebestky et al, 2003;Crozatier et al, 2004;Mandal et al, 2007;Minakhina et al, 2007Minakhina et al, , 2011Sinenko et al, 2009;Pennetier et al, 2012;Dragojlovic-Munther and Martinez-Agosto, 2013;Ferguson and Martinez-Agosto, 2014;Milton et al, 2014;Destalminil-Letourneau et al, 2021). In contrast, under unchallenged conditions, the lymph gland disintegrates and releases all of its hemocytes at the beginning of metamorphosis (Grigorian et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Macrophages and Their Organ Locations Shape Each Other in Development and Homeostasis – A Drosophila Perspective

Mase

Augsburger

Brückner

2021

Front. Cell Dev. Biol.

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Across the animal kingdom, macrophages are known for their functions in innate immunity, but they also play key roles in development and homeostasis. Recent insights from single cell profiling and other approaches in the invertebrate model organism Drosophila melanogaster reveal substantial diversity among Drosophila macrophages (plasmatocytes). Together with vertebrate studies that show genuine expression signatures of macrophages based on their organ microenvironments, it is expected that Drosophila macrophage functional diversity is shaped by their anatomical locations and systemic conditions. In vivo evidence for diverse macrophage functions has already been well established by Drosophila genetics: Drosophila macrophages play key roles in various aspects of development and organogenesis, including embryogenesis and development of the nervous, digestive, and reproductive systems. Macrophages further maintain homeostasis in various organ systems and promote regeneration following organ damage and injury. The interdependence and interplay of tissues and their local macrophage populations in Drosophila have implications for understanding principles of organ development and homeostasis in a wide range of species.

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The vascular niche controls Drosophila hematopoiesis via fibroblast growth factor signaling

Cited by 27 publications

References 62 publications

Ubx-Collier signaling cascade maintains blood progenitors in the posterior lobes of the Drosophila larval lymph gland

Ubx-Collier signaling cascade maintains blood progenitors in the posterior lobes of the Drosophila larval lymph gland

Drosophila as a Model to Study Cellular Communication Between the Hematopoietic Niche and Blood Progenitors Under Homeostatic Conditions and in Response to an Immune Stress

Macrophages and Their Organ Locations Shape Each Other in Development and Homeostasis – A Drosophila Perspective

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