Relish plays a dynamic role in the niche to modulate Drosophila blood progenitor homeostasis in development and infection.

Parvathy Ramesh,Aditya Kanwal,Sudip Mandal,Lolitika Mandal,Nidhi Sharma Dey

doi:10.7554/elife.67158

Parvathy Ramesh, Aditya Kanwal + Show 3 more

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https://doi.org/10.7554/elife.67158

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Abstract

Immune challenges demand the gearing up of basal hematopoiesis to combat infection. Little is known about how during development, this switch is achieved to take care of the insult. Here, we show that the hematopoietic niche of the larval lymph gland of Drosophila senses immune challenge and reacts to it quickly through the nuclear factor-κB (NF-κB), Relish, a component of the immune deficiency (Imd) pathway. During development, Relish is triggered by ecdysone signaling in the hematopoietic niche to maintain the blood progenitors. Loss of Relish causes an alteration in the cytoskeletal architecture of the niche cells in a Jun Kinase-dependent manner, resulting in the trapping of Hh implicated in progenitor maintenance. Notably, during infection, downregulation of Relish in the niche tilts the maintenance program toward precocious differentiation, thereby bolstering the cellular arm of the immune response.

Highlights

The larval blood-forming organ, the lymph gland, is the site for definitive hematopoiesis in Drosophila (Banerjee et al, 2019; Evans et al, 2003; Jung et al, 2005; Lanot et al, 2001; Mandal et al, 2004)
The innermost core progenitors are maintained by the adjacent cardiac cells that serve as niche (Destalminil-Letourneau et al, 2021), while the bulk of primed progenitors are maintained by the posterior signaling center (PSC) or the niche (Baldeosingh et al, 2018; Sharma et al, 2019)
We found that 107 Relish acts as an inhibitor of c-Jun Kinase Signaling (JNK) in the hematopoietic niche

Summary

Introduction

The larval blood-forming organ, the lymph gland, is the site for definitive hematopoiesis in Drosophila (Banerjee et al, 2019; Evans et al, 2003; Jung et al, 2005; Lanot et al, 2001; Mandal et al, 2004). The hematopoietic niche maintains the delicate balance between the number of progenitors and differentiated cells of the lymph gland (Baldeosingh et al, 2018; Krzemień et al, 2007; Mandal et al, 2007; Sharma et al, 2019). During development, this organ accumulates hemocytes for post-larval requirements. Though the candidate that breaks the maintenance circuit remains to be identified, our study illustrates that the hematopoietic niche can sense the physiological state of an animal to facilitate a transition from normal to emergency hematopoiesis

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