Migration ofDrosophilaintestinal stem cells across organ boundaries

Abstract

All components of the Drosophila intestinal tract, including the endodermal midgut and ectodermal hindgut/Malpighian tubules, maintain populations of dividing stem cells. In the midgut and hindgut, these stem cells originate from within larger populations of intestinal progenitors that proliferate during the larval stage and form the adult intestine during metamorphosis. The origin of stem cells found in the excretory Malpighian tubules (‘renal stem cells’) has not been established. In this paper, we investigate the migration patterns of intestinal progenitors that take place during metamorphosis. Our data demonstrate that a subset of adult midgut progenitors (AMPs) move posteriorly to form the adult ureters and, consecutively, the renal stem cells. Inhibiting cell migration by AMP-directed expression of a dominant-negative form of Rac1 protein results in the absence of stem cells in the Malpighian tubules. As the majority of the hindgut progenitor cells migrate posteriorly and differentiate into hindgut enterocytes, a group of the progenitor cells, unexpectedly, invades anteriorly into the midgut territory. Consequently, these progenitor cells differentiate into midgut enterocytes. The midgut determinant GATAe is required for the differentiation of midgut enterocytes derived from hindgut progenitors. Wingless signaling acts to balance the proportion of hindgut progenitors that differentiate as midgut versus hindgut enterocytes. Our findings indicate that a stable boundary between midgut and hindgut/Malpighian tubules is not established during early embryonic development; instead, pluripotent progenitor populations cross in between these organs in both directions, and are able to adopt the fate of the organ in which they come to reside.

All for one and one for all: Regionalization of the Drosophila intestine

“…Contrary to other midgut stem cells, GaSCs are grouped in a cluster throughout life within the cardia at the foregut-midgut junction and do not spread throughout the epithelium within the different compartments. Similar ISC behavior is observed at the midgut-hindgut junction (Fox and Spradling, 2009;Takashima et al, 2013Takashima et al, , 2008. Differences in the ISC division rate are also observed.…”

“…Additionally, the adult midgut is populated after the proliferation in late larval stages of adult midgut progenitors (AMPs), which are grouped in nests along the larval midgut and spread to colonize the transient pupal and future adult midgut (H. Mathur et al, 2010;Micchelli et al, 2011;Takashima et al, 2011). At the pupal stage, these adult midgut progenitors can still be exchanged between the hindgut and midgut, indicating that precursor's identity is not predetermined during larval or early pupal stages (Takashima et al, 2011(Takashima et al, , 2013. However, in the case of the adult middle midgut, the specification of the copper cell region occurs during a defined window of metamorphosis.…”

Metamorphosis of the Drosophila visceral musculature and its role in intestinal morphogenesis and stem cell formation

“…The epithelial layer of the hindgut and foregut is also replaced by a new set of adult cells. In contrast to the midgut, progenitors of the adult foregut and hindgut are integrated in the larval epithelium, where they form narrow, cylindrical domains at the boundaries between foregut/midgut, and hindgut/midgut, respectively (Singh et al, 2011; Takashima et al, 2008; 2013). The process by which progenitors of the adult foregut and hindgut proliferate, spread out to replace the larval enterocytes, and become ensheathed by visceral muscles has not been documented previously, and will be analyzed in the present study.…”

Hexapoda: A Drosophila’s View of Development

“…1.35C , blue arrowhead; Takashima et al 2013 ). Upon these cells, though derived from the ectodermal (according to current defi nitions) HPZ, express all phenotypic aspects of midgut enterocytes.…”