The eggshell of Drosophila melanogaster. V. Structure and morphogenesis of the micropylar apparatus

1986 ◽  
Vol 64 (11) ◽  
pp. 2509-2519 ◽  
Author(s):  
Flora E. Zarani ◽  
Lukas H. Margaritis

The micropylar apparatus in Drosophila melanogaster consists of two parts. The inner part is a protrusion of vitelline membrane, whereas the outer part is a chorionic protrusion containing a canal, through which the spermatozoon enters. In the formation of the micropylar apparatus two follicle cell subpopulations are involved: the border cells, i.e., a group of 9 follicle cells, and the peripheral cells (about 36 cells). The morphogenesis of the micropyle starts at stage 10B, when the border cells secrete the paracrystalline region of the vitelline membrane. The micropylar canal (length 7 μm, diameter 0.7 μm) and the pocket that penetrates within the paracrystalline structure are moulded by two border cell projections, full of microtubules. The formation of the micropyle terminates at stage 14B, when its chorionic part is completed and the border cell projections degenerate. The structure of the micropyle in fertilized and unfertilized laid eggs differs from the mature (stage 14B) egg in that the vitelline membrane is modified and appears homogeneous as in the rest of the eggshell. These transformations seem to be unrelated to sperm entry.

1964 ◽  
Vol s3-105 (70) ◽  
pp. 209-212
Author(s):  
R. C. KING

A centripetal migration of follicle cells, which results in a separation of egg and nurse chambers, occurs in higher dipterans like Drosophila melanogaster but not in lower dipterans like Anopheles maculipennis. In Anopheles and Drosophila, while the vitelline membrane can be secreted in the absence of the oocyte, the follicle cells must be present. This suggests that the follicle cell is the governing agent in the synthesis of the vitelline membrane. The envelopes of Drosophila embryos differ from those surrounding ovarian eggs in that a membrane about 0.04 µ thick lies directly outside the vitelline membrane. This thin layer is thought to represent a waterproofing wax which forms once the egg leaves the ovariole.


1963 ◽  
Vol s3-104 (67) ◽  
pp. 297-320
Author(s):  
R. C. KING ◽  
ELIZABETH A. KOCH

Studies are described of the ultrastructure of the follicle cells which invest the oocyte of Drosophila melanogaster at the time of vitelline membrane formation. Of particular interest are organelles made up of endoplasmic reticulum organized into a husk of concentric lamellae which surround lipidal droplets. These epithelial bodies are seen only at the time the vitelline membrane is being formed, and it is assumed therefore that the lipidal material of the epithelial body may be utilized somehow in the fabrication of the vitelline membrane. Cytochemical studies have shown this membrane to contain at least 5 classes of compounds; a protein, two lipids (which may be distinguished by differences in their resistance to extraction by various solvents), and 2 polysaccharides (1 neutral and 1 acidic). Studies were made of vitelline membrane formation in the ovaries of flies homozygous for either of 2 recessive, female-sterile genes (tiny and female sterile). In the case of the ty mutation vitelline membrane material is sometimes secreted between follicle and nurse cells, while in the mutant fes vitelline membrane is observed in rare instances to be secreted between follicle cells and an adjacent layer of tumour cells. In the latter case the vitelline membrane shows altered cytochemical properties. The fact that vitelline membrane can be secreted by follicle cells not adjacent to an oocyte demonstrates that it is the follicle cell rather than the oocyte that plays the major role in the secretion of the precursor material of the vitelline membrane. Subsequently the follicle cells secrete the egg-shell, or chorion, which is subdivided into a dense, compartmented, inner endochorion, and a pale, outer exochorion. A description is given of the ultrastructure of the follicle cells during the secretion of the endochorion and the exochorion. The endochorion contains a protein, a polysaccharide, and a lipid, all of which may be distinguished cytochemically from the vitelline membrane compounds. The exochorion contains large amounts of acidic mucopolysaccharides. Specialized follicle cells form the micropylar apparatus and the chorionic appendages. The formation of the chorion and chorionic appendages is discussed in the light of information gained from abnormalities of the chorions and chorionic appendages seen in ty and fs 2.1 oocytes. Subsequent to the time the egg leaves the ovariole a layer of waterproofing wax is secreted between the vitelline membrane and the chorion.


Development ◽  
1995 ◽  
Vol 121 (8) ◽  
pp. 2255-2263 ◽  
Author(s):  
A.M. Murphy ◽  
T. Lee ◽  
C.M. Andrews ◽  
B.Z. Shilo ◽  
D.J. Montell

To investigate the molecular mechanisms responsible for the temporal and spatial control of cell movements during development, we have been studying the migration of a small group of follicle cells, called the border cells, in the Drosophila ovary. Timely initiation of border cell migration requires the product of the slow border cells (slbo) locus, which encodes the Drosophila homolog of the transcription factor C/EBP. Here we report evidence that one target of C/EBP in the control of border cell migration is the FGF receptor homolog encoded by the breathless (btl) locus. btl expression in the ovary was border cell-specific, beginning just prior to the migration, and this expression was reduced in slbo mutants. btl mutations dominantly enhanced the border cell migration defects found in weak slbo alleles. Furthermore, C/EBP-independent btl expression was able to rescue the migration defects of hypomorphic slbo alleles. Purified Drosophila C/EBP bound eight sites in the btl 5′ flanking region by DNAse I footprinting. Taken together these results suggest that btl is a key, direct target for C/EBP in the regulation of border cell migration.


1999 ◽  
Vol 144 (3) ◽  
pp. 533-547 ◽  
Author(s):  
Paulina Niewiadomska ◽  
Dorothea Godt ◽  
Ulrich Tepass

Cadherins are involved in a variety of morphogenetic movements during animal development. However, it has been difficult to pinpoint the precise function of cadherins in morphogenetic processes due to the multifunctional nature of cadherin requirement. The data presented here indicate that homophilic adhesion promoted by Drosophila E-cadherin (DE-cadherin) mediates two cell migration events during Drosophila oogenesis. In Drosophila follicles, two groups of follicle cells, the border cells and the centripetal cells migrate on the surface of germline cells. We show that the border cells migrate as an epithelial patch in which two centrally located cells retain epithelial polarity and peripheral cells are partially depolarized. Both follicle cells and germline cells express DE-cadherin, and border cells and centripetal cells strongly upregulate the expression of DE-cadherin shortly before and during their migration. Removing DE-cadherin from either the follicle cells or the germline cells blocks migration of border cells and centripetal cells on the surface of germline cells. The function of DE-cadherin in border cells appears to be specific for migration as the formation of the border cell cluster and the adhesion between border cells are not disrupted in the absence of DE-cadherin. The speed of migration depends on the level of DE-cadherin expression, as border cells migrate more slowly when DE-cadherin activity is reduced. Finally, we show that the upregulation of DE-cadherin expression in border cells depends on the activity of the Drosophila C/EBP transcription factor that is essential for border cell migration.


2020 ◽  
Author(s):  
Haifa Alhadyian ◽  
Dania Shoiab ◽  
Robert E. Ward

AbstractProtein components of the invertebrate occluding junction - known as the septate junction (SJ) - are required for morphogenetic developmental events during embryogenesis in Drosophila melanogaster. In order to determine whether SJ proteins are similarly required for morphogenesis during other developmental stages, we investigated the localization and requirement of four representative SJ proteins during oogenesis: Contactin, Macroglobulin complement-related, Neurexin IV, and Coracle. A number of morphogenetic processes occur during oogenesis, including egg elongation, formation of dorsal appendages, and border cell migration. We found that all four SJ proteins are expressed in the egg throughout oogenesis, with the highest and most sustained levels in the follicular epithelium (FE). In the FE, SJ proteins localize along the lateral membrane during early and mid-oogenesis, but become enriched in an apical-lateral domain (the presumptive SJ) by stage 10b. SJ protein relocalization requires the expression of other SJ proteins, as well as rab5 and rab11 in a manner similar to SJ biogenesis in the embryo. Knocking down the expression of these SJ proteins in follicle cells throughout oogenesis results in egg elongation defects and abnormal dorsal appendages. Similarly, reducing the expression of SJ genes in the border cell cluster results in border cell migration defects. Together, these results demonstrate an essential requirement for SJ genes in morphogenesis during oogenesis, and suggests that SJ proteins may have conserved functions in epithelial morphogenesis across developmental stages.Article SummarySeptate junction (SJ) proteins are essential for forming an occluding junction in epithelial tissues of Drosophila melanogaster. SJ proteins are also required for morphogenetic events during embryogenesis prior to the formation of an occluding junction. To determine if SJ proteins function in morphogenesis at other developmental stages, we examined their function during oogenesis, and found that SJ proteins are expressed in the follicular epithelium of the egg chamber and are required for egg elongation, dorsal appendages formation, and border cell migration. Additionally, we found that the formation of SJs in oogenesis is similar to that in embryonic epithelia.


Development ◽  
2002 ◽  
Vol 129 (22) ◽  
pp. 5131-5140 ◽  
Author(s):  
Muriel Grammont ◽  
Kenneth D. Irvine

Patterning of the Drosophila egg requires the establishment of several distinct types of somatic follicle cells, as well as interactions between these follicle cells and the oocyte. The polar cells occupy the termini of the follicle and are specified by the activation of Notch. We have investigated their role in follicle patterning by creating clones of cells mutant for the Notch modulator fringe. This genetic ablation of polar cells results in cell fate defects within surrounding follicle cells. At the anterior, the border cells, the immediately adjacent follicle cell fate, are absent, as are the more distant stretched and centripetal follicle cells. Conversely, increasing the number of polar cells by expressing an activated form of the Notch receptor increases the number of border cells. At the posterior, elimination of polar cells results in abnormal oocyte localization. Moreover, when polar cells are mislocalized laterally, the surrounding follicle cells adopt a posterior fate, the oocyte is located adjacent to them,and the anteroposterior axis of the oocyte is re-oriented with respect to the ectopic polar cells. Our observations demonstrate that the polar cells act as an organizer that patterns surrounding follicle cells and establishes the anteroposterior axis of the oocyte. The origin of asymmetry duringDrosophila development can thus be traced back to the specification of the polar cells during early oogenesis.


1984 ◽  
Vol 67 (1) ◽  
pp. 87-119
Author(s):  
D.L. Bishop ◽  
R.C. King

Females homozygous for the otu7 allele produce ovarian tumours, as well as egg chambers that reach a relatively late stage of development. Mutant ovarian nurse cells contain giant polytene chromosomes. These are transcriptionally active, and RNA is transported to the oocyte through ring canals, although at reduced rate. Vitellogenic oocytes are endocytotically active. Protein (alpha yolk) spheres are formed, but glycogen (beta yolk) spheres were never seen in the ooplasm. Follicle cells migrate normally and secrete more vitelline membrane and chorion than is required to cover the slowly growing oocyte. Specialized follicle cells also secrete relatively normal dorsal appendages. The micropylar cone is secreted by another cluster of specialized follicle cells called border cells. These are out of phase with the oocyte, and the forming micropylar cone prevents the nurse cells from passing the remainder of their cytoplasm to the oocyte. The result is a morphologically abnormal chamber blocked at the p-12 stage. Sections through the micropylar cone of a p-12 chamber demonstrated that one of the border cells formed a projection containing a bundle of microtubules. Secretions of the border cells were deposited against this tube, which later degenerates or is withdrawn. Normally this results in a canal, the micropyle, through which the sperm enters the egg. The slowed growth of the mutant oocyte presumably results from a defect in the transport of fluids or charged molecules to it, and the otu+ gene is therefore believed to play a vital role in this process.


Development ◽  
1996 ◽  
Vol 122 (2) ◽  
pp. 409-418 ◽  
Author(s):  
T. Lee ◽  
L. Feig ◽  
D.J. Montell

Receptor tyrosine kinases have been shown to promote cell movement in a variety of systems. The Ras protein, a well-documented downstream effector for receptor tyrosine kinases, may contribute to receptor tyrosine kinase-mediated motility. In the present study, we have examined the role of Ras in the migration of a small subset of follicle cells, known as the border cells, during Drosophila oogenesis. A dominant-negative Ras protein inhibited cell migration when expressed specifically in border cells during the period when these cells normally migrate. When expressed prior to migration, dominant-negative Ras promoted premature initiation of migration. Conversely, expression of constitutively active Ras prior to migration resulted in a significant delay in the initiation step. Furthermore, the defect in initiation of border cell migration found in slbo1, a mutation at the locus that encodes Drosophila C/EBP, was largely rescued by reducing Ras activity in border cells prior to migration. Taken together, these observations indicate that Ras activity plays two distinct roles in the border cells: (1) reduction in Ras activity promotes the initiation of that migration process and (2) Ras activity is required during border cell migration. We further examined the possible involvement of two downstream effectors of Ras in border cell migration. Raf activity was dispensable to border cell migration while reduced Ral activity inhibited initiation. We therefore suggest that Ras plays a critical role in the dynamic regulation of border cell migration via a Raf-independent pathway.


Development ◽  
1965 ◽  
Vol 13 (2) ◽  
pp. 215-233
Author(s):  
Ruth Bellairs

In the adult hen each oöcyte is surrounded by a capsule of follicle cells and all the raw materials that enter the oöcyte must pass through this capsule. It is not surprising, therefore, that the morphological relationships between the follicle and the oöcyte are of a highly specialized nature. Several workers have studied them, mainly by light microscopy, but their findings have not been unanimous, largely because of difficulties in resolving fine details. For instance, although it has frequently been suggested that certain structures pass from the follicle cell into the oöcyte, these structures have been interpreted by different authors as Golgi bodies, as mitochondria or as fat drops. Similarly, there have been several different theories about the relationship between the cell membrane of the oöcyte, the zona radiata and the vitelline membrane.


1999 ◽  
Vol 146 (5) ◽  
pp. 1075-1086 ◽  
Author(s):  
Daniela C. Zarnescu ◽  
Graham H. Thomas

Changes in cell shape and position drive morphogenesis in epithelia and depend on the polarized nature of its constituent cells. The spectrin-based membrane skeleton is thought to be a key player in the establishment and/or maintenance of cell shape and polarity. We report that apical βHeavy-spectrin (βH), a terminal web protein that is also associated with the zonula adherens, is essential for normal epithelial morphogenesis of the Drosophila follicle cell epithelium during oogenesis. Elimination of βH by the karst mutation prevents apical constriction of the follicle cells during mid-oogenesis, and is accompanied by a gross breakup of the zonula adherens. We also report that the integrity of the migratory border cell cluster, a group of anterior follicle cells that delaminates from the follicle epithelium, is disrupted. Elimination of βH prevents the stable recruitment of α-spectrin to the apical domain, but does not result in a loss of apicobasal polarity, as would be predicted from current models describing the role of spectrin in the establishment of cell polarity. These results demonstrate a direct role for apical (αβH)2-spectrin in epithelial morphogenesis driven by apical contraction, and suggest that apical and basolateral spectrin do not play identical roles in the generation of apicobasal polarity.


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