Dual role for Jumu in the control of hematopoietic progenitors in the Drosophila lymph gland.

Yangguang Hao,Li Hua Jin

doi:10.7554/elife.25094

Abstract

The Drosophila lymph gland is a hematopoietic organ in which the maintenance of hematopoietic progenitor cell fate relies on intrinsic factors and extensive interaction with cells within a microenvironment. The posterior signaling center (PSC) is required for maintaining the balance between progenitors and their differentiation into mature hemocytes. Moreover, some factors from the progenitors cell-autonomously control blood cell differentiation. Here, we show that Jumeau (Jumu), a member of the forkhead (Fkh) transcription factor family, controls hemocyte differentiation of lymph gland through multiple regulatory mechanisms. Jumu maintains the proper differentiation of prohemocytes by cell-autonomously regulating the expression of Col in medullary zone and by non-cell-autonomously preventing the generation of expanded PSC cells. Jumu can also cell-autonomously control the proliferation of PSC cells through positive regulation of dMyc expression. We also show that a deficiency of jumu throughout the lymph gland can induce the differentiation of lamellocytes via activating Toll signaling.

Highlights

The development and specification of blood cells in humans and Drosophila are controlled by conserved transcriptional regulators and signaling pathways
To further analyze the function of Jumu in larval hematopoietic homeostasis, we first detected the expression of the plasmatocyte marker P1, the crystal cell marker Hindsight (Hnt) and the lamellocyte marker L1 in the lymph glands of jumu mutants
We found that the activation of the Toll pathway throughout the through the overexpression of Toll10b under the control of Srp-Gal4 caused a robust increase in the lamellocyte in more than 80% of the lymph glands (n = 30), and led to enrichment of Dorsal-related immunity factor (Dif) in the nuclear in the medullary zone (MZ) and cortical zone (CZ) without affecting the Dorsal expression and localization (Figure 9N,T; Figure 9—figure supplement 2G,G’)

Summary

Introduction

The development and specification of blood cells in humans and Drosophila are controlled by conserved transcriptional regulators and signaling pathways. The first population of hemocytes is derived from the embryonic head mesoderm and provides two types of circulating blood cells, plasmatocytes and crystal cells (Holz et al, 2003). The second wave of hematopoiesis occurs during the larval stage in a specialized hematopoietic organ known as the lymph gland (Lanot et al, 2001). At the onset of metamorphosis, the lymph gland breaks down, releasing plasmatocytes and crystal cells into the circulating hemolymph (Crozatier and Vincent, 2011). The primary lobes are organized in three zones: the cortical zone (CZ) contains differentiated hemocytes, the medullary zone (MZ) is composed of prohemocytes, and the posterior signaling center (PSC) functions as a hematopoietic niche for maintaining a population of blood cell precursors (Jung et al, 2005).

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Conclusion