Evidence for a highly selective RNA transport system and its role in establishing the dorsoventral axis of the Drosophila egg

Development ◽  
1992 ◽  
Vol 114 (3) ◽  
pp. 653-661 ◽  
Author(s):  
H.K. Cheung ◽  
T.L. Serano ◽  
R.S. Cohen
Keyword(s):  
Dorsal Surface ◽  
Drosophila Embryo ◽  
Follicle Cells ◽  
Oocyte Nucleus ◽  
Axis Formation ◽  
Asymmetric Distribution ◽  
Rna Transport ◽  
Nurse Cells ◽  
Dorsoventral Axis ◽  
Multistep Process

The specification of cell fates along the dorsoventral axis of the Drosophila embryo is dependent on the asymmetric distribution of proteins within the egg and within the egg's outer membranes. Such asymmetries arise during oogenesis and are dependent on multiple cell-cell interactions between the developing oocyte and its neighboring somatic follicle cells. The earliest known such interaction involves the generation of a signal in the oocyte and its reception in the follicle cells lying on the dorsal surface of the oocyte at approximately stage 10 of oogenesis. Several independent lines of investigation indicate that the fs(1)K10 (K10) gene negatively regulates the synthesis of the signal in the oocyte nucleus. Here we present data that indicate that the accumulation of K10 protein in the oocyte nucleus is a multistep process involving: (1) the synthesis of K10 RNA in nurse cells, (2) the rapid transport of K10 RNA from nurse cells into the oocyte, (3) the localization of K10 RNA to the anterior margin of the oocyte, and (4) K10 protein synthesis and localization. K10 RNA is transported into the oocyte continuously beginning at approximately stage 2. This indicates a high degree of selectivity in transport, since most RNAs synthesized in stage 2 and older nurse cells are stored there until stage 11, when nurse cells donate their entire cytoplasm to the oocyte. The sequences responsible for the early (pre-stage 11) and selective transport of K10 RNA into the oocyte map to the 3' transcribed non-translated region of the gene. None of the other identified genes involved in dorsoventral axis formation are required for K10 RNA transport.(ABSTRACT TRUNCATED AT 250 WORDS)

maelstrom is required for an early step in the establishment of Drosophila oocyte polarity: posterior localization of grk mRNA

Development ◽  
1997 ◽  
Vol 124 (22) ◽  
pp. 4661-4671 ◽  
Author(s):  
N.J. Clegg ◽  
D.M. Frost ◽  
M.K. Larkin ◽  
L. Subrahmanyan ◽  
Z. Bryant ◽  
...  
Keyword(s):  
Nurse Cell ◽  
Egf Receptor ◽  
Mrna Localization ◽  
Follicle Cells ◽  
Rna Transport ◽  
Nurse Cells ◽  
Loss Of Function ◽  
Cell Fates ◽  
Early Step ◽  
Novel Protein

We describe a mutant, maelstrom, that disrupts a previously unobserved step in mRNA localization within the early oocyte, distinct from nurse-cell-to-oocyte RNA transport. Mutations in maelstrom disturb the localization of mRNAs for Gurken (a ligand for the Drosophila Egf receptor), Oskar and Bicoid at the posterior of the developing (stage 3–6) oocyte. maelstrom mutants display phenotypes detected in gurken loss-of-function mutants: posterior follicle cells with anterior cell fates, bicoid mRNA localization at both poles of the stage 8 oocyte and ventralization of the eggshell. These data are consistent with the suggestion that early posterior localization of gurken mRNA is essential for activation of the Egf receptor pathway in posterior follicle cells. Posterior localization of mRNA in stage 3–6 oocytes could therefore be one of the earliest known steps in the establishment of oocyte polarity. The maelstrom gene encodes a novel protein that has a punctate distribution in the cytoplasm of the nurse cells and the oocyte until the protein disappears in stage 7 of oogenesis.

scholarly journals Mirror represses pipe expression in follicle cells to initiate dorsoventral axis formation in Drosophila

Development ◽  
2012 ◽  
Vol 139 (6) ◽  
pp. 1110-1114 ◽  
Author(s):  
M. J. Andreu ◽  
E. Gonzalez-Perez ◽  
L. Ajuria ◽  
N. Samper ◽  
S. Gonzalez-Crespo ◽  
...  
Keyword(s):  
Follicle Cells ◽  
Axis Formation ◽  
Dorsoventral Axis

Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes

Development ◽  
1997 ◽  
Vol 124 (24) ◽  
pp. 4927-4937 ◽  
Author(s):  
A. Gonzalez-Reyes ◽  
H. Elliott ◽  
D. St Johnston
Keyword(s):  
Symmetry Breaking ◽  
Germinal Vesicle ◽  
Follicle Cells ◽  
Axis Formation ◽  
Main Body ◽  
Nurse Cells ◽  
Egg Chambers ◽  
Anterior Posterior ◽  
Oocyte Selection

The two main body axes in Drosophila become polarised as a result of a series of symmetry-breaking steps during oogenesis. Two of the sixteen germline cells in each egg chamber develop as pro-oocytes, and the first asymmetry arises when one of these cells is selected to become the oocyte. Anterior-posterior polarity originates when the oocyte then comes to lie posterior to the nurse cells and signals through the Gurken/Egfr pathway to induce the adjacent follicle cells to adopt a posterior fate. This directs the movement of the germinal vesicle and associated gurken mRNA from the posterior to an anterior corner of the oocyte, where Gurken protein signals for a second time to induce the dorsal follicle cells, thereby polarising the dorsal-ventral axis. Here we describe a group of five genes, the spindle loci, which are required for each of these polarising events. spindle mutants inhibit the induction of both the posterior and dorsal follicle cells by disrupting the localisation and translation of gurken mRNA. Moreover, the oocyte often fails to reach the posterior of mutant egg chambers and differentiates abnormally. Finally, double mutants cause both pro-oocytes to develop as oocytes, by delaying the choice between these two cells. Thus, these mutants reveal a novel link between oocyte selection, oocyte positioning and axis formation in Drosophila, leading us to propose that the spindle genes act in a process that is common to several of these events.

scholarly journals INTERCELLULAR MIGRATION OF CENTRIOLES IN THE GERMARIUM OF DROSOPHILA MELANOGASTER

1970 ◽  
Vol 45 (2) ◽  
pp. 306-320 ◽  
Author(s):  
Anthony P. Mahowald ◽  
Joan M. Strassheim
Keyword(s):  
Follicle Cell ◽  
Cell Cluster ◽  
Follicle Cells ◽  
Oocyte Nucleus ◽  
Nurse Cells ◽  
Serial Sections ◽  
Cell Border ◽  
Ring Canals ◽  
Egg Chambers ◽  
Stage 1

A cluster of centrioles has been found in the early Drosophila oocyte. Since the oocyte is connected to 15 nurse cells by a system of intercellular bridges or ring canals, the possibility that the cluster of centrioles arose in the germarium from an intercellular migration of centrioles from the nurse cells to the oocyte was analyzed in serial sections for the electron microscope. Initially, all of the 16 cells of the future egg chambers possess centrioles, which are located in a juxtanuclear position. At the time the 16 cell cluster becomes arranged in a lens-shaped layer laterally across the germarium, the centrioles lose their juxtanuclear position and move towards the oocyte. By the time the 16 cell cluster of cells is surrounded by follicle cells (Stage 1), between 14 and 17 centrioles are found in the oocyte. Later, these centrioles become located between the oocyte nucleus and the follicle cell border and become aggregated into a cluster less than 1.5 µ in its largest dimension. The fate of these centrioles in the oocyte is not known. The fine structure of the germarium and the early oocyte is also described.

scholarly journals mago nashi mediates the posterior follicle cell-to-oocyte signal to organize axis formation in Drosophila

Development ◽  
1997 ◽  
Vol 124 (16) ◽  
pp. 3197-3207 ◽  
Author(s):  
P.A. Newmark ◽  
S.E. Mohr ◽  
L. Gong ◽  
R.E. Boswell
Keyword(s):  
Germ Plasm ◽  
Egf Receptor ◽  
Germ Line ◽  
Follicle Cell ◽  
Posterior Pole ◽  
Follicle Cells ◽  
Oocyte Nucleus ◽  
Axis Formation ◽  
Pole Plasm ◽  
Mago Nashi

Establishment of the anteroposterior and dorsoventral axes in the Drosophila egg chamber requires reciprocal signaling between the germ line and soma. Upon activation of the Drosophila EGF receptor in the posterior follicle cells, these cells signal back to the oocyte, resulting in a reorganization of the oocyte cytoplasm and anterodorsal migration of the oocyte nucleus. We demonstrate that the gene mago nashi (mago) encodes an evolutionarily conserved protein that must be localized within the posterior pole plasm for germ-plasm assembly and Caenorhabditis elegans mago is a functional homologue of Drosophila mago. In the absence of mago+ function during oogenesis, the anteroposterior and dorsoventral coordinates of the oocyte are not specified and the germ plasm fails to assemble.

Dorsoventral axis formation in Drosophila depends on the correct dosage of the gene gurken

Development ◽  
1994 ◽  
Vol 120 (9) ◽  
pp. 2457-2463 ◽  
Author(s):  
F.S. Neuman-Silberberg ◽  
T. Schupbach
Keyword(s):  
Germ Line ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Limiting Factor ◽  
Axis Formation ◽  
Dorsoventral Patterning ◽  
Wild Type ◽  
Cell Fates ◽  
Dorsoventral Axis ◽  
Signaling Process

The Drosophila gene gurken participates in a signaling process that occurs between the germ line and the somatic cells (follicle cells) of the ovary. This process is required for correct patterning of the dorsoventral axis of both the egg and the embryo. gurken produces a spatially localized transcript which encodes a TGF-alpha-like molecule (Neuman-Silberberg and Schupbach, Cell 75, 165–174, 1993). Mutations in gurken cause a ventralized phenotype in egg and embryo. To determine whether the gurken gene product plays an instructive role in dorsoventral patterning, we constructed females containing extra copies of a gurken transgene. Such females produce dorsalized eggs and embryos, which is expected if gurken acts as a limiting factor in the dorsoventral patterning process. In addition, the expression pattern of the gene rhomboid in the follicle cells is altered in ovaries of females containing extra copies of gurken. Our results indicate that changing gurken dosage in otherwise wild-type ovaries is sufficient to alter the number of somatic follicle cells directed to the dorsal fate. Therefore the gurken-torpedo signaling process plays an instructive role in oogenesis. It induces dorsal cell fates in the follicle cell epithelium and it controls the production of maternal components that will direct the embryonic dorsoventral pattern after fertilization.

Mechanisms of Gurken-dependentpiperegulation and the robustness of dorsoventral patterning inDrosophila

Development ◽  
2002 ◽  
Vol 129 (12) ◽  
pp. 2965-2975 ◽  
Author(s):  
Francesca Peri ◽  
Martin Technau ◽  
Siegfried Roth
Keyword(s):  
Egf Receptor ◽  
Follicle Cell ◽  
Dorsal Side ◽  
Drosophila Embryo ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Axis Formation ◽  
Embryonic Patterning ◽  
Cell Fates ◽  
Egg Chamber

The restriction of Pipe, a potential glycosaminoglycan-modifying enzyme, to ventral follicle cells of the egg chamber is essential for dorsoventral axis formation in the Drosophila embryo. pipe repression depends on the TGFα-like ligand Gurken, which activates the Drosophila EGF receptor in dorsal follicle cells. An analysis of Raf mutant clones shows that EGF signalling is required cell-autonomously in all dorsal follicle cells along the anteroposterior axis of the egg chamber to repress pipe. However, the autoactivation of EGF signalling important for dorsal follicle cell patterning has no influence on pipe expression. Clonal analysis shows that also the mirror-fringe cassette suggested to establish a secondary signalling centre in the follicular epithelium is not involved in pipe regulation. These findings support the view that the pipe domain is directly delimited by a long-range Gurken gradient. Pipe induces ventral cell fates in the embryo via activation of the Spätzle/Toll pathway. However, large dorsal patches of ectopic pipe expression induced by Raf clones rarely affect embryonic patterning if they are separated from the endogenous pipe domain. This indicates that potent inhibitory processes prevent pipe dependent Toll activation at the dorsal side of the egg.

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