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

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.

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

Development ◽

10.1242/dev.114.3.653 ◽

1992 ◽

Vol 114 (3) ◽

pp. 653-661 ◽

Cited By ~ 14

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)

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Faculty Opinions recommendation of Coupling of rotational cortical flow, asymmetric midbody positioning, and spindle rotation mediates dorsoventral axis formation in C. elegans.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718276783.793492693 ◽

2014 ◽

Author(s):

Rik Korswagen

Keyword(s):

Axis Formation ◽

Dorsoventral Axis ◽

C Elegans ◽

Spindle Rotation

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Faculty Opinions recommendation of Coupling of rotational cortical flow, asymmetric midbody positioning, and spindle rotation mediates dorsoventral axis formation in C. elegans.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718276783.793491320 ◽

2014 ◽

Author(s):

Xueliang Zhu

Keyword(s):

Axis Formation ◽

Dorsoventral Axis ◽

C Elegans ◽

Spindle Rotation

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Dorsoventral Axis Formation in the Drosophila Embryo—Shaping and Transducing a Morphogen Gradient

Current Biology ◽

10.1016/j.cub.2005.10.026 ◽

2005 ◽

Vol 15 (21) ◽

pp. R887-R899 ◽

Cited By ~ 157

Author(s):

Bernard Moussian ◽

Siegfried Roth

Keyword(s):

Drosophila Embryo ◽

Morphogen Gradient ◽

Axis Formation ◽

Dorsoventral Axis

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Sequential activation of the EGF receptor pathway during Drosophila oogenesis establishes the dorsoventral axis

Development ◽

10.1242/dev.125.2.191 ◽

1998 ◽

Vol 125 (2) ◽

pp. 191-200 ◽

Cited By ~ 10

Author(s):

A. Sapir ◽

R. Schweitzer ◽

B.Z. Shilo

Keyword(s):

Target Genes ◽

Egf Receptor ◽

Ectopic Expression ◽

Follicle Cell ◽

Follicle Cells ◽

Cell Fates ◽

Dorsoventral Axis ◽

Spatial Coordinates ◽

Sequential Activation

Previous work has demonstrated a role for the Drosophila EGF receptor (Torpedo/DER) and its ligand, Gurken, in the determination of anterioposterior and dorsoventral axes of the follicle cells and oocyte. The roles of DER in establishing the polarity of the follicle cells were examined further, by following the expression of DER-target genes. One class of genes (e.g. kekon) is induced by the DER pathway at all stages. Broad expression of kekon at the stage in which the follicle cells migrate posteriorly over the oocyte, demonstrates the capacity of the pathway to pattern all follicle cells except the ventral-most rows. This may provide the spatial coordinates for the ventral-most follicle cell fates. A second group of target genes (e.g. rhomboid (rho)) is induced only at later stages of oogenesis, and may require additional inputs by signals emanating from the anterior, stretch follicle cells. The function of Rho was analyzed by ectopic expression in the stretch follicle cells, and shown to induce a non-autonomous dorsalizing activity that is independent of Gurken. Rho thus appears to be involved in processing a DER ligand in the follicle cells, to pattern the egg chamber and allow persistent activation of the DER pathway during formation of the dorsal appendages.

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Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila oogenesis

Development ◽

10.1242/dev.125.15.2837 ◽

1998 ◽

Vol 125 (15) ◽

pp. 2837-2846 ◽

Cited By ~ 13

Author(s):

A. Gonzalez-Reyes ◽

D. St Johnston

Keyword(s):

Follicle Cell ◽

Cell Types ◽

Follicle Cells ◽

Follicular Epithelium ◽

Axis Formation ◽

Main Body ◽

Drosophila Oogenesis ◽

Egfr Mutant ◽

Anterior Posterior ◽

Anterior Posterior Axis

Gurken signals from the oocyte to the adjacent follicle cells twice during Drosophila oogenesis; first to induce posterior fate, thereby polarising the anterior-posterior axis of the future embryo and then to induce dorsal fate and polarise the dorsal-ventral axis. Here we show that Gurken induces two different follicle cell fates because the follicle cells at the termini of the egg chamber differ in their competence to respond to Gurken from the main-body follicle cells in between. By removing the putative Gurken receptor, Egfr, in clones of cells, we show that Gurken signals directly to induce posterior fate in about 200 cells, defining a terminal competence domain that extends 10–11 cell diameters from the pole. Furthermore, small clones of Egfr mutant cells at the posterior interpret their position with respect to the pole and differentiate as the appropriate anterior cell type. Thus, the two terminal follicle cell populations contain a symmetric prepattern that is independent of Gurken signalling. These results suggest a three-step model for the anterior-posterior patterning of the follicular epithelium that subdivides this axis into at least five distinct cell types. Finally, we show that Notch plays a role in both the specification and patterning of the terminal follicle cells, providing a possible explanation for the defect in anterior-posterior axis formation caused by Notch and Delta mutants.

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