scholarly journals Septate junction proteins are required for egg elongation and border cell migration during oogenesis in Drosophila

2020 ◽  
Author(s):  
Haifa Alhadyian ◽  
Dania Shoiab ◽  
Robert E. Ward
Keyword(s):  
Drosophila Melanogaster ◽  
Cell Migration ◽  
Developmental Stages ◽  
Septate Junction ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Essential Requirement ◽  
Border Cell ◽  
Border Cell Migration ◽  
Protein Components

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.

scholarly journals Septate junction proteins are required for egg elongation and border cell migration during oogenesis in Drosophila

2021 ◽  
Author(s):  
Haifa Alhadyian ◽  
Dania Shoaib ◽  
Robert E Ward
Keyword(s):  
Drosophila Melanogaster ◽  
Cell Migration ◽  
Developmental Stages ◽  
Septate Junction ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Border Cell ◽  
Egg Chambers ◽  
Border Cell Migration ◽  
Protein Components

Abstract Protein 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 egg chambers 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 Summary: Septate junction (SJ) proteins are essential for forming an occluding junction in epithelial tissues in Drosophila melanogaster, and also for morphogenetic events that occur prior to the formation of the junction during embryogenesis. Here we show that SJ proteins are expressed in the follicular epithelium of egg chambers during oogenesis and are required for morphogenetic events including egg elongation, dorsal appendages formation, and border cell migration. Additionally, the formation of SJs during oogenesis is similar to that in embryonic epithelia.

The breathless FGF receptor homolog, a downstream target of Drosophila C/EBP in the developmental control of cell migration

Development ◽  
1995 ◽  
Vol 121 (8) ◽  
pp. 2255-2263 ◽  
Author(s):  
A.M. Murphy ◽  
T. Lee ◽  
C.M. Andrews ◽  
B.Z. Shilo ◽  
D.J. Montell
Keyword(s):  
Cell Migration ◽  
Molecular Mechanisms ◽  
Follicle Cells ◽  
Border Cells ◽  
Timely Initiation ◽  
Fgf Receptor ◽  
Border Cell ◽  
Downstream Target ◽  
Border Cell Migration ◽  
Factor C

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.

Two distinct roles for Ras in a developmentally regulated cell migration

Development ◽  
1996 ◽  
Vol 122 (2) ◽  
pp. 409-418 ◽  
Author(s):  
T. Lee ◽  
L. Feig ◽  
D.J. Montell
Keyword(s):  
Cell Migration ◽  
Tyrosine Kinases ◽  
Receptor Tyrosine Kinases ◽  
Critical Role ◽  
Dominant Negative ◽  
Follicle Cells ◽  
Border Cells ◽  
Ras Protein ◽  
Border Cell ◽  
Border Cell Migration

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.

scholarly journals Hypoxia response pathway in border cell migration

2010 ◽  
Vol 4 (3) ◽  
pp. 391-395 ◽  
Author(s):  
Inna Djagaeva ◽  
Sergey Doronkin
Keyword(s):  
Cell Migration ◽  
Hypoxia Response ◽  
Border Cell ◽  
Border Cell Migration

Two actions of juvenile hormone on the follicle cells of Rhodnius prolixus Stål

1975 ◽  
Vol 53 (8) ◽  
pp. 1187-1188 ◽  
Author(s):  
Randa Abu-Hakima ◽  
K. G. Davey
Keyword(s):  
Juvenile Hormone ◽  
Developmental Stages ◽  
Normal Animal ◽  
Rhodnius Prolixus ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Intercellular Spaces

The follicular epithelium of vitellogenic oocytes from allatectomized females of Rhodnius fails to develop large intercellular spaces when exposed to juvenile hormone (JH) in vitro. This suggests that in the normal animal, the follicle cells require JH at two developmental stages. Differentiation of the cells in the presence of JH represents one requirement, and only those cells which have undergone this initial priming are fully competent to exhibit the second response, the development of intercellular spaces.

Jing: a downstream target of slbo required for developmental control of border cell migration

Development ◽  
2001 ◽  
Vol 128 (3) ◽  
pp. 321-330 ◽  
Author(s):  
Y. Liu ◽  
D.J. Montell
Keyword(s):  
Cell Migration ◽  
Leucine Zipper ◽  
Inducible Promoter ◽  
Regulatory Sequence ◽  
Border Cells ◽  
Border Cell ◽  
Downstream Target ◽  
Border Cell Migration ◽  
Factor C ◽  
Drosophila Ovary

Epithelial to mesenchymal transitions and cell migration are important features of embryonic development and tumor metastasis. We are employing a systematic genetic approach to study the border cells in the Drosophila ovary, as a simple model for these cellular behaviors. Previously we found that expression of the basic-region/leucine zipper transcription factor, C/EBP, is required for the border cells to initiate their migration. Here we report the identification of a second nuclear factor, named JING (which means ‘still’), that is required for initiation of border cell migration. The jing locus was identified in a screen for mutations that cause border cell migration defects in mosaic clones. The jing mutant phenotype resembles that of slbo mutations, which disrupt the Drosophila C/EBP gene, but is distinct from other classes of border cell migration mutants. Expression of a jing-lacZ reporter in border cells requires C/EBP. Moreover, expression of jing from a heat-inducible promoter rescues the border cell migration defects of hypomorphic slbo mutants. The JING protein is most closely related to a mouse protein, AEBP2, which was identified on the basis of its ability to bind a small regulatory sequence within the adipocyte AP2 gene to which mammalian C/EBP also binds. We propose that the need to coordinate cell differentiation with nutritional status may be the link between mammalian adipocytes and Drosophila border cells that led to the conservation of C/EBP and AEBP2.

scholarly journals The ETS-transcription factor Pointed is sufficient to regulate the posterior fate of the follicular epithelium

Development ◽  
2020 ◽  
Vol 147 (22) ◽  
pp. dev189787
Author(s):  
Cody A. Stevens ◽  
Nicole T. Revaitis ◽  
Rumkan Caur ◽  
Nir Yakoby
Keyword(s):  
Transcription Factor ◽  
Growth Factor Receptor ◽  
Bmp Signaling ◽  
Janus Kinase ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
T Box ◽  
Border Cell ◽  
Morphogenetic Protein ◽  
Ets Transcription Factor

ABSTRACTThe Janus-kinase/signal transducer and activator of transcription (JAK/STAT) pathway regulates the anterior posterior axis of the Drosophila follicle cells. In the anterior, it activates the bone morphogenetic protein (BMP) signaling pathway through expression of the BMP ligand decapentaplegic (dpp). In the posterior, JAK/STAT works with the epidermal growth factor receptor (EGFR) pathway to express the T-box transcription factor midline (mid). Although MID is necessary for establishing the posterior fate of the egg chamber, we show that it is not sufficient to determine a posterior fate. The ETS-transcription factor pointed (pnt) is expressed in an overlapping domain to mid in the follicle cells. This study shows that pnt is upstream of mid and that it is sufficient to induce a posterior fate in the anterior end, which is characterized by the induction of mid, the prevention of the stretched cells formation and the abrogation of border cell migration. We demonstrate that the anterior BMP signaling is abolished by PNT through dpp repression. However, ectopic DPP cannot rescue the anterior fate formation, suggesting additional targets of PNT participate in the posterior fate determination.

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