scholarly journals Prostaglandins regulate invasive, collective border cell migration

2019 ◽  
Author(s):  
Emily F. Fox ◽  
Maureen C. Lamb ◽  
Samuel Q. Mellentine ◽  
Tina L. Tootle
Keyword(s):  
Cell Migration ◽  
Genetic Interaction ◽  
Mechanisms Of Action ◽  
Nurse Cells ◽  
Wild Type ◽  
Significant Delay ◽  
Border Cell ◽  
Border Cell Migration ◽  
Co Reduction ◽  
Cluster Length

AbstractWhile prostaglandins (PGs), short-range lipid signals, regulate cell migration, their mechanisms of action are poorly understood in collective migration. To address this, we useDrosophilaborder cell migration during Stage 9 of oogenesis. The border cells delaminate from the epithelium, and migrate collectively and invasively between the nurse cells. Pxt is theDrosophilacyclooxygenase-like enzyme responsible for all PG synthesis. Loss of Pxt results in both a significant delay in border cell migration during Stage 9 and an increase in cluster length compared to wild-type controls. Contributing to these phenotypes is altered integrin localization. Integrins are enriched on the border cell membranes, and this enrichment is lost inpxtmutants. Active integrins require interaction with the actin cytoskeleton. As we previously found PGs regulate the actin bundler Fascin and Fascin is required for border cell migration, we hypothesized PGs regulate Fascin to control integrins. Supporting this, loss of Fascin results in apxt-like integrin localization, and dominant genetic interaction studies reveal that co-reduction of Pxt and Fascin results in delayed and elongated border cell clusters. Together these data lead to the model that PG signaling controls Fascin, and thereby integrins, to mediate on-time border cell migration and maintain cluster cohesion.

scholarly journals Nuclear lamins promote protrusion dynamics and collective, confined migration in vivo

2021 ◽  
Author(s):  
Lauren Penfield ◽  
Denise Montell
Keyword(s):  
Cell Migration ◽  
Nurse Cells ◽  
Border Cells ◽  
Collective Migration ◽  
Cell Nuclei ◽  
Migration Path ◽  
Border Cell ◽  
Nuclear Lamins ◽  
Border Cell Migration

Cells migrate collectively through confined environments during development and cancer metastasis. While the nucleus, a large and stiff organelle, impedes cell migration between non-deformable pillars in vitro, its function in vivo may vary depending on the microenvironment. Further, it is unknown how nuclei contribute to collective migration in vivo and whether nuclei in different positions within cell collectives experience different forces. Here, we use border cell migration in the fly ovary as an in vivo model to investigate the effects of confined, collective migration on nuclei and the contribution of nuclear lamins to migration. We found severe yet transient nuclear deformations occur, particularly in the leading cell, as border cells squeeze through tiny crevices between germline cells, termed nurse cells. Leading cells extend protrusions between nurse cells, which may pry open space to allow the cluster to advance. Here we report that the leading cell nuclei deformed as they moved into leading protrusions. Then as protrusions widened, the nucleus recovered a more circular shape. These data suggest that lead cell nuclei may help protrusions expand and thereby enlarge the migration path. To test how nuclei might promote or impede border cell migration, we investigated nuclear lamins, proteins that assemble into intermediate filaments and structurally support the nuclear envelope. Depletion of the Drosophila B-type lamin, Lam, from the outer, motile border cells, but not the inner, nonmotile polar cells, impeded border cell migration, whereas perturbations of the A-type lamin, LamC, did not. While wild type border cell clusters typically have one large leading protrusion as they delaminate from the anterior follicular epithelium, clusters depleted of B-type lamin had multiple, short-lived protrusions, resulting in unproductive cluster movement and failure to progress along the migration path. Further, border cell nuclei depleted of B-type lamins were small, formed blebs, and ruptured. Together, these data indicate that B-type lamin is requied for nuclear integrity, which in turn stabilizes the leading protrusion and promotes overall cluster polarization and collective movement through confined spaces.

scholarly journals Fascin regulates protrusions and delamination to mediate invasive, collective cell migration in vivo

2019 ◽  
Author(s):  
Maureen C. Lamb ◽  
Kelsey K. Anliker ◽  
Tina L. Tootle
Keyword(s):  
Cell Migration ◽  
Cancer Metastasis ◽  
Collective Cell Migration ◽  
Nurse Cells ◽  
Border Cells ◽  
Border Cell ◽  
Migration Data ◽  
Border Cell Migration

AbstractFascin is an actin bundling protein that is essential for developmental cell migrations and promotes cancer metastasis. In addition to bundling actin, Fascin has several actin-independent roles. Border cell migration during Drosophila oogenesis provides an excellent model to study Fascin’s various roles during invasive, collective cell migration. Border cell migration requires Fascin. Fascin functions not only within the migrating border cells, but also within the nurse cells, the substrate for this migration. Loss of Fascin results in increased, shorter and mislocalized protrusions during migration. Data supports the model that Fascin promotes the activity of Enabled, an actin elongating factor, to regulate migration. Additionally, loss of Fascin inhibits border cell delamination. These defects are partially due to altered E-cadherin localization in the border cells; this is predicted to be an actin-independent role of Fascin. Overall, Fascin is essential for multiple aspects of this invasive, collective cell migration, and functions in both actin-dependent and -independent manners. These findings have implications beyond Drosophila, as border cell migration has emerged as a model to study mechanisms mediating cancer metastasis.

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

Breaking a temporal barrier: signalling crosstalk regulates the initiation of border cell migration

2009 ◽  
Vol 11 (5) ◽  
pp. 536-538 ◽  
Author(s):  
Dorothea Godt ◽  
Ulrich Tepass
Keyword(s):  
Cell Migration ◽  
Border Cell ◽  
Border Cell Migration

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.

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 Spatial restriction of receptor tyrosine kinase activity through a polarized endocytic cycle controls border cell migration

2010 ◽  
Vol 107 (52) ◽  
pp. 22558-22563 ◽  
Author(s):  
G. Assaker ◽  
D. Ramel ◽  
S. K. Wculek ◽  
M. Gonzalez-Gaitan ◽  
G. Emery
Keyword(s):  
Cell Migration ◽  
Tyrosine Kinase ◽  
Receptor Tyrosine Kinase ◽  
Kinase Activity ◽  
Tyrosine Kinase Activity ◽  
Border Cell ◽  
Border Cell Migration

scholarly journals A role for the chaperone Hsp70 in the regulation of border cell migration in the Drosophila ovary

2008 ◽  
Vol 125 (11-12) ◽  
pp. 1048-1058 ◽  
Author(s):  
Laura Cobreros ◽  
Ana Fernández-Miñán ◽  
Carlos M. Luque ◽  
Acaimo González-Reyes ◽  
María D. Martín-Bermudo
Keyword(s):  
Cell Migration ◽  
Border Cell ◽  
Border Cell Migration ◽  
Drosophila Ovary ◽  
Chaperone Hsp70
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