Abstract
BackgroundThe Drosophila egg chamber provides an excellent system in which to study the specification and differentiation of epithelial cell fates because all of the steps, starting with the division of the corresponding stem cells, called follicle stem cells, have been well described and occur many times over in a single ovary.Methodology/Principal FindingsHere we investigate the role of the small Rab11 GTPase in follicle stem cells (FSCs) and in their differentiating daughters, which include main body epithelial cells, stalk cells and polar cells. We show that rab11-null FSCs maintain their ability to self renew, even though previous studies have shown that FSC self renewal is dependent on maintenance of E-cadherin-based intercellular junctions, which in many cell types, including Drosophila germline stem cells, requires Rab11. We also show that rab11-null FSCs give rise to normal numbers of cells that enter polar, stalk, and epithelial cell differentiation pathways, but that none of the cells complete their differentiation programs and that the epithelial cells undergo premature programmed cell death. Finally we show, through the induction of rab11-null clones at later points in the differentiation program, that Rab11 suppresses tumor-like growth of epithelial cells. Thus, rab11-null epithelial cells arrest differentiation early, assume an aberrant cell morphology, delaminate from the epithelium, and invade the neighboring germline cyst. These phenotypes are associated with defects in E-cadherin localization and a general loss of cell polarity.Conclusions/SignificanceWhile previous studies have revealed tumor suppressor or tumor suppressor-like activity for regulators of endocytosis, our study is the first to identify such activity for regulators of endocytic recycling. Our studies also support the recently emerging view that distinct mechanisms regulate junction stability and plasticity in different tissues.
Highlights
The Drosophila oocyte develops within a highly organized group of cells called the egg chamber
After secretion of these coverings, the epithelial and nurse cells are targeted for programmed cell death (PCD), leaving the mature egg behind, which is passed through the oviduct and fertilized
We used the FRT-FLP system, to generate rab11-null clones that were marked by the loss of nuclear GFP (Methods)
Summary
The Drosophila oocyte develops within a highly organized group of cells called the egg chamber. Two FSCs (green) reside at the germarial region 2a/2b junction and give rise to undifferentiated pre-follicle cells (white) and three types of differentiated follicle cells: epithelial (grey), polar (red) and stalk (blue). (F, F9) Control rab11-null; P[rab11+] clones in an s8 egg chamber immunostained for nGFP (green) and Eya (red).
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