Oskar anchoring restricts pole plasm formation to the posterior of the Drosophila oocyte

Development ◽  
2002 ◽  
Vol 129 (15) ◽  
pp. 3705-3714 ◽  
Author(s):  
Nathalie F. Vanzo ◽  
Anne Ephrussi
Keyword(s):  
Drosophila Melanogaster ◽  
Translational Control ◽  
Cell Formation ◽  
Positional Information ◽  
Mrna Localization ◽  
Posterior Pole ◽  
Tight Coupling ◽  
Anteroposterior Patterning ◽  
Pole Cell ◽  
Pole Plasm

Localization of the maternal determinant Oskar at the posterior pole of Drosophila melanogaster oocyte provides the positional information for pole plasm formation. Spatial control of Oskar expression is achieved through the tight coupling of mRNA localization to translational control, such that only posterior-localized oskar mRNA is translated, producing the two Oskar isoforms Long Osk and Short Osk. We present evidence that this coupling is not sufficient to restrict Oskar to the posterior pole of the oocyte. We show that Long Osk anchors both oskar mRNA and Short Osk, the isoform active in pole plasm assembly, at the posterior pole. In the absence of anchoring by Long Osk, Short Osk disperses into the bulk cytoplasm during late oogenesis, impairing pole cell formation in the embryo. In addition, the pool of untethered Short Osk causes anteroposterior patterning defects, owing to the dispersion of pole plasm and its abdomen-inducing activity throughout the oocyte. We show that the N-terminal extension of Long Osk is necessary but not sufficient for posterior anchoring, arguing for multiple docking elements in Oskar. This study reveals cortical anchoring of the posterior determinant Oskar as a crucial step in pole plasm assembly and restriction, required for proper development of Drosophila melanogaster.

Drosophila virilis oskar transgenes direct body patterning but not pole cell formation or maintenance of mRNA localization in D. melanogaster

Development ◽  
1994 ◽  
Vol 120 (7) ◽  
pp. 2027-2037 ◽  
Author(s):  
P.J. Webster ◽  
J. Suen ◽  
P.M. Macdonald
Keyword(s):  
Drosophila Melanogaster ◽  
Germ Cell ◽  
Cell Formation ◽  
Mrna Localization ◽  
Early Embryo ◽  
Posterior Pole ◽  
Early Embryogenesis ◽  
Drosophila Virilis ◽  
Pole Cell ◽  
Body Patterning

The Drosophila melanogaster gene oskar is required for both posterior body patterning and germline formation in the early embryo; precisely how oskar functions is unknown. The oskar transcript is localized to the posterior pole of the developing oocyte, and oskar mRNA and protein are maintained at the pole through early embryogenesis. The posterior maintenance of oskar mRNA is dependent upon the presence of oskar protein. We have cloned and characterized the Drosophila virilis oskar homologue, virosk, and examined its activity as a transgene in Drosophila melanogaster flies. We find that the cis-acting mRNA localization signals are conserved, although the virosk transcript also transiently accumulates at novel intermediate sites. The virosk protein, however, shows substantial differences from oskar: while virosk is able to rescue body patterning in a D. melanogaster oskar- background, it is impaired in both mRNA maintenance and pole cell formation. Furthermore, virosk induces a dominant maternal-effect lethality when introduced into a wild-type background, and interferes with the posterior maintenance of the endogenous oskar transcript in early embryogenesis. Our data suggest that virosk protein is unable to anchor at the posterior pole of the early embryo; this defect could account for all of the characteristics of virosk mentioned above. Our observations support a model in which oskar protein functions both by nucleating the factors necessary for the activation of the posterior body patterning determinant and the germ cell determinant, and by anchoring these factors to the posterior pole of the embryo. While the posterior body patterning determinant need not be correctly localized to provide body patterning activity, the germ cell determinant may need to be highly concentrated adjacent to the cortex in order to direct pole cell formation.

scholarly journals Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole

2001 ◽  
Vol 154 (3) ◽  
pp. 511-524 ◽  
Author(s):  
Fredericus J.M. van Eeden ◽  
Isabel M. Palacios ◽  
Mark Petronczki ◽  
Matthew J.D. Weston ◽  
Daniel St Johnston
Keyword(s):  
Germ Cells ◽  
Translational Control ◽  
Mrna Localization ◽  
Posterior Pole ◽  
Rna Transport ◽  
Specific Component ◽  
Microtubule Cytoskeleton ◽  
Transport Complex ◽  
Pole Plasm ◽  
Null Mutants

The localization of Oskar at the posterior pole of the Drosophila oocyte induces the assembly of the pole plasm and therefore defines where the abdomen and germ cells form in the embryo. This localization is achieved by the targeting of oskar mRNA to the posterior and the localized activation of its translation. oskar mRNA seems likely to be actively transported along microtubules, since its localization requires both an intact microtubule cytoskeleton and the plus end–directed motor kinesin I, but nothing is known about how the RNA is coupled to the motor. Here, we describe barentsz, a novel gene required for the localization of oskar mRNA. In contrast to all other mutations that disrupt this process, barentsz-null mutants completely block the posterior localization of oskar mRNA without affecting bicoid and gurken mRNA localization, the organization of the microtubules, or subsequent steps in pole plasm assembly. Surprisingly, most mutant embryos still form an abdomen, indicating that oskar mRNA localization is partially redundant with the translational control. Barentsz protein colocalizes to the posterior with oskar mRNA, and this localization is oskar mRNA dependent. Thus, Barentsz is essential for the posterior localization of oskar mRNA and behaves as a specific component of the oskar RNA transport complex.

aubergineencodes aDrosophilapolar granule component required for pole cell formation and related to eIF2C

Development ◽  
2001 ◽  
Vol 128 (14) ◽  
pp. 2823-2832 ◽  
Author(s):  
Adam N. Harris ◽  
Paul M. Macdonald
Keyword(s):  
Polar Granule ◽  
Cell Formation ◽  
Posterior Pole ◽  
Translation Initiation Factor ◽  
Initiation Factor ◽  
Dependent Manner ◽  
Eukaryotic Translation ◽  
Pole Cell ◽  
Body Patterning ◽  
Pole Plasm

In Drosophila oocytes, activation of Oskar translation from a transcript localized to the posterior pole is an essential step in the organization of the pole plasm, specialized cytoplasm that contains germline and abdominal body patterning determinants. Oskar is a component of polar granules, large particles associated with the pole plasm and the germline precursor pole cells of the embryo. aubergine mutants fail to translate oskar mRNA efficiently and are thus defective in posterior body patterning and pole cell formation. We have found that Aubergine protein is related to eukaryotic translation initiation factor 2C and suggest how it may activate translation. In addition, we found that Aubergine was recruited to the posterior pole in a vas-dependent manner and is itself a polar granule component. Consistent with its presence in these structures, Aubergine is required for pole cell formation independently of its initial role in oskar translation. Unlike two other known polar granule components, Vasa and Oskar, Aubergine remains cytoplasmic after pole cell formation, suggesting that the roles of these proteins diverge during embryogenesis.

Differentiation and positioning of nuclei in eggs of the cecidomyid Heteropeza pygmaea

1976 ◽  
Vol 22 (1) ◽  
pp. 99-113
Author(s):  
M. Meats ◽  
J.B. Tucker
Keyword(s):  
Structural Changes ◽  
Early Stage ◽  
Cell Formation ◽  
Longitudinal Axis ◽  
Posterior Pole ◽  
Spindle Orientation ◽  
Specific Sequence ◽  
Pole Cell ◽  
Polar Granules ◽  
Egg Chamber

During the first three cleavage divisions of the egg nuclei a precise sequence of spindle orientation and elongation parallel to the longitudinal axis of the egg is apparently involved in positioning one nucleus among the polar granules at the posterior pole of the egg. The size of this nucleus, and the position at which the egg cleaves when pole cell formation occurs, appear to constitute part of the mechanism which ensures that only one nucleus is included in the first pole cell. Blastoderm formation occurs without a well-defined migration of nuclei to the egg surface. Nuclei are so large in relation to the size of the egg that uniform spacing and distribution of nuclei ensures that a large proportion are situated near the egg surface. Those nuclei which are near the egg surface divide synchronously to form a layer of blastoderm nuclei, while membranous cleavage furrows invaginate from the egg surface between them. Nuclei in the central region of the egg chamber condense to form yolk nuclei before blastoderm nuclei have been separated from the rest of the egg by the completion of the cleavage membranes. Polar granules provide the only evidence of fine-structural differences in different regions of the egg chamber cytoplasm. They are found near the posterior pole of the egg from an early stage of oogenesis. They undergo a specific sequence of structural changes and increase in size as the egg grows. No microtubular or microfibrillar arrays have been found in the egg chamber which might form a cytoskeletal basis for spindle orientation or for the spatial differences which develop during differentiation of the uncleaved egg cytoplasm.

Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly

Development ◽  
1995 ◽  
Vol 121 (11) ◽  
pp. 3723-3732 ◽  
Author(s):  
F.H. Markussen ◽  
A.M. Michon ◽  
W. Breitwieser ◽  
A. Ephrussi
Keyword(s):  
Positive Feedback ◽  
Translational Control ◽  
Feedback Mechanism ◽  
Posterior Pole ◽  
Start Codon ◽  
Anterior Pole ◽  
Wild Type ◽  
Alternative Start Codon ◽  
Positive Feedback Mechanism ◽  
Pole Plasm

At the posterior pole of the Drosophila oocyte, oskar induces a tightly localized assembly of pole plasm. This spatial restriction of oskar activity has been thought to be achieved by the localization of oskar mRNA, since mislocalization of the RNA to the anterior induces anterior pole plasm. However, ectopic pole plasm does not form in mutant ovaries where oskar mRNA is not localized, suggesting that the unlocalized mRNA is inactive. As a first step towards understanding how oskar activity is restricted to the posterior pole, we analyzed oskar translation in wild type and mutants. We show that the targeting of oskar activity to the posterior pole involves two steps of spatial restriction, cytoskeleton-dependent localization of the mRNA and localization-dependent translation. Furthermore, our experiments demonstrate that two isoforms of Oskar protein are produced by alternative start codon usage. The short isoform, which is translated from the second in-frame AUG of the mRNA, has full oskar activity. Finally, we show that when oskar RNA is localized, accumulation of Oskar protein requires the functions of vasa and tudor, as well as oskar itself, suggesting a positive feedback mechanism in the induction of pole plasm by oskar.

Pole cell formation in Drosophila melanogaster

1980 ◽  
Vol 75 (2) ◽  
pp. 419-430 ◽  
Author(s):  
Margaret MacMorris Swanson ◽  
Clifton A. Poodry
Keyword(s):  
Drosophila Melanogaster ◽  
Cell Formation ◽  
Pole Cell

scholarly journals An Interaction Type of Genetic Screen Reveals a Role of the Rab11 Gene in oskar mRNA Localization in the Developing Drosophila melanogaster Oocyte

Genetics ◽  
2001 ◽  
Vol 158 (3) ◽  
pp. 1177-1188
Author(s):  
Ferenc Jankovics ◽  
Rita Sinka ◽  
Miklós Erdélyi
Keyword(s):  
Drosophila Melanogaster ◽  
Mrna Localization ◽  
Posterior Pole ◽  
Genetic Screen ◽  
Transport Processes ◽  
Follicle Cells ◽  
Actin Binding ◽  
Interaction Type ◽  
Microtubule Organization ◽  
Microtubule Network

Abstract Abdomen and germ cell development of Drosophila melanogaster embryo requires proper localization of oskar mRNA to the posterior pole of the developing oocyte. oskar mRNA localization depends on complex cell biological events like cell-cell communication, dynamic rearrangement of the microtubule network, and function of the actin cytoskeleton of the oocyte. To investigate the cellular mechanisms involved, we developed a novel interaction type of genetic screen by which we isolated 14 dominant enhancers of a sensitized genetic background composed of mutations in oskar and in TropomyosinII, an actin binding protein. Here we describe the detailed analysis of two allelic modifiers that identify Drosophila Rab11, a gene encoding small monomeric GTPase. We demonstrate that mutation of the Rab11 gene, involved in various vesicle transport processes, results in ectopic localization of oskar mRNA, whereas localization of gurken and bicoid mRNAs and signaling between the oocyte and the somatic follicle cells are unaffected. We show that the ectopic oskar mRNA localization in the Rab11 mutants is a consequence of an abnormally polarized oocyte microtubule cytoskeleton. Our results indicate that the internal membranous structures play an important role in the microtubule organization in the Drosophila oocyte and, thus, in oskar RNA localization.

scholarly journals Experimental Studies on Pole Cells and Midgut Differentiation in Diptera

1960 ◽  
Vol 13 (4) ◽  
pp. 541 ◽  
Author(s):  
DF Poulson ◽  
DF Waterhouse
Keyword(s):  
Drosophila Melanogaster ◽  
Germ Cells ◽  
Polar Region ◽  
Experimental Studies ◽  
Cell Formation ◽  
Lucilia Cuprina ◽  
Pole Cell ◽  
Gonad Size ◽  
The Common ◽  
Pole Cells

Highly localized irradiation with ultraviolet of the posterior polar region of eggs of Drosophila melanogaster and Lucilia cuprina in pre.pole cell and pole cell stages results in reduction in numbers of the cuprophilic cells of the middle midgut as well as in reduction of gonad size and number. Carefully timed eggs were exposed to dosages of ultraviolet (from a source giving about 90 per cent. at wavelength 2536 A) ranging from 1200 to 2400 I-' W sec/cm2 over periods of 2-4 min. Treatments at the time of active pole cell formation were found to be most effective in producing defects of both gut and gonads, thus demon� strating the common origin of the cuprophilic cells of the middle midgut and the germ cells of the gonads.

The fat facets gene is required for Drosophila eye and embryo development

Development ◽  
1992 ◽  
Vol 116 (4) ◽  
pp. 985-1000 ◽  
Author(s):  
J.A. Fischer-Vize ◽  
G.M. Rubin ◽  
R. Lehmann
Keyword(s):  
Amino Acids ◽  
Germ Cell ◽  
Protein Function ◽  
Cell Formation ◽  
Posterior Pole ◽  
Hybrid Protein ◽  
Drosophila Eye ◽  
Fat Facets ◽  
Pole Plasm ◽  
Germ Cell Formation

In a screen for mutations affecting Drosophila eye development, we have identified a gene called fat facets (faf) which is required for cell interactions that prevent particular cells in the developing eye from becoming photoreceptors. Analysis of eyes mosaic for faf+ and faf- cells shows that faf is required in cells near to, but outside, normal developing photoreceptors and also outside of the ectopic photoreceptors in mutant facets. faf is also essential during oogenesis, and we show that a faf-lacZ hybrid protein is localized via the first 392 amino acids of faf to the posterior pole of oocytes. Posterior localization of faf-lacZ depends on oskar. oskar encodes a key organizer of the pole plasm, a specialized cytoplasm at the posterior pole of embryos. The pole plasm is required for germ cell formation and contains the determinant of posterior polarity, encoded by nanos. Although other pole plasm components are required for localization of nanos RNA or for nanos protein function, faf is not. We have cloned the faf gene, and have shown that it encodes two similar large (approximately 300 × 10(3) M(r)) proteins that are unique with respect to other known proteins.

Sign in / Sign up

Export Citation Format

Share Document