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Drosophila border cells

Afsoon Saadin, Michelle Starz-Gaiano
Drosophila border cells undergo a straightforward and stereotypical collective migration during egg development. However, a complex genetic program underlies this process. A variety of approaches, including biochemical, genetic, and imaging strategies have identified many regulatory components, revealing layers of control. This complexity suggests that the active processes of evaluating the environment, remodeling the cytoskeleton, and coordinating movements among cells, demand rapid systems for modulating cell behaviors...
October 2016: Trends in Genetics: TIG
Marcus Michel, Maryam Aliee, Katrin Rudolf, Lisa Bialas, Frank Jülicher, Christian Dahmann
The separation of cells with distinct fates and functions is important for tissue and organ formation during animal development. Regions of different fates within tissues are often separated from another along straight boundaries. These compartment boundaries play a crucial role in tissue patterning and growth by stably positioning organizers. In Drosophila, the wing imaginal disc is subdivided into a dorsal and a ventral compartment. Cells of the dorsal, but not ventral, compartment express the selector gene apterous...
2016: PloS One
Julia Lautemann, Johannes Bohrmann
BACKGROUND: Ion-transport mechanisms and gap junctions are known to cooperate in creating bioelectric phenomena, like pH gradients, voltage gradients and ion fluxes within single cells, tissues, organs, and whole organisms. Such phenomena have been shown to play regulatory roles in a variety of developmental and regenerative processes. Using Drosophila oogenesis as a model system, we aim at characterizing in detail the mechanisms underlying bioelectric phenomena in order to reveal their regulatory functions...
July 13, 2016: BMC Developmental Biology
Aeri Cho, Masato Kato, Tess Whitwam, Ji Hoon Kim, Denise J Montell
A longstanding mystery has been the absence of cytoplasmic intermediate filaments (IFs) from Drosophila despite their importance in other organisms. In the course of characterizing the in vivo expression and functions of Drosophila Tropomyosin (Tm) isoforms, we discovered an essential but unusual product of the Tm1 locus, Tm1-I/C, which resembles an IF protein in some respects. Like IFs, Tm1-I/C spontaneously forms filaments in vitro that are intermediate in diameter between F-actin and microtubules. Like IFs but unlike canonical Tms, Tm1-I/C contains N- and C-terminal low-complexity domains flanking a central coiled coil...
July 26, 2016: Cell Reports
Michael T Veeman, Jocelyn A McDonald
Tissues in developing embryos exhibit complex and dynamic rearrangements that shape forming organs, limbs, and body axes. Directed migration, mediolateral intercalation, lumen formation, and other rearrangements influence the topology and topography of developing tissues. These collective cell behaviors are distinct phenomena but all involve the fine-grained control of cell polarity. Here we review recent findings in the dynamics of polarized cell behavior in both the Drosophila ovarian border cells and the Ciona notochord...
2016: F1000Research
Wei Dai, Denise J Montell
Border cells are a cluster of cells that migrate from the anterior tip of the Drosophila egg chamber to the border of the oocyte in stage 9. They serve as a useful model to study collective cell migration in a native tissue environment. Here we describe a protocol for preparing ex vivo egg chamber cultures from transgenic flies expressing fluorescent proteins in the border cells, and using confocal microscopy to take a multi-positional time-lapse movie. We include an image analysis method for tracking border cell cluster dynamics as well as tracking individual cell movements...
2016: Methods in Molecular Biology
Ginés Morata, Salvador C Herrera
We discuss recent work about cellular reprogramming during regeneration of the imaginal discs of Drosophila. These contain various lineage blocks, compartments, which express distinct genetic programmes. It has been found that after massive damage to a compartment cells from a neighbour compartment can transgress the compartment border and contribute to its regeneration. The transgressing cells are genetically reprogrammed and acquire a new identity, a process facilitated by up regulation of the JNK pathway and transient loss of epigenetic control by the Pc-G and trx-G genes...
October 2016: Current Opinion in Genetics & Development
Dan Wang, Lingyun Li, Juan Lu, Suning Liu, Jie Shen
Animal morphogenesis requires folds or clefts to separate populations of cells which are often associated with different cell affinities. In the Drosophila wing imaginal disc, the regional expression of the Iroquois complex (Iro-C) in the notum leads to the formation of the hinge/notum (H/N) fold that separates the wing hinge and notum territories. Although Decapentaplegic (Dpp) signaling has been revealed as essential for the hinge/notum subdivision through the restriction of Iro-C toward the notum region, the mechanism by which the H/N border develops into a fold is unknown...
August 1, 2016: Developmental Biology
Afsoon Saadin, Michelle Starz-Gaiano
The Janus Kinase/Signal Transducer and Activator of Transcription (JAK/STAT) signaling pathway is an essential regulator of cell migration both in mammals and fruit flies. Cell migration is required for normal embryonic development and immune response but can also lead to detrimental outcomes, such as tumor metastasis. A cluster of cells termed "border cells" in the Drosophila ovary provides an excellent example of a collective cell migration, in which two different cell types coordinate their movements. Border cells arise within the follicular epithelium and are required to invade the neighboring cells and migrate to the oocyte to contribute to a fertilizable egg...
2016: G3: Genes—Genomes—Genetics
E V Marylovtseva, L V Omelyanchuk
Hepatocyte growth factor receptor tyrosine kinase substrate (Hrs) is an endosome protein involved in the sorting and transport of receptor tyrosine kinases and other proteins (which are absorbed by the cell during endocytosis) from early endosomes to lysosomes. Since receptor tyrosine kinases are important components of different cellular signaling systems, Hrs protein defects can result in the appearance of a number of developmental anomalies. In particular, it was demonstrated that ectopic Hrs expression in the wing kidney results in the disappearance of one or several rows of marginal wing setae in imago (which indicates hrs gene involvement in the development of the disc D/V border)...
October 2015: Genetika
Lauren Anllo, Trudi Schüpbach
Cell migration plays crucial roles during development. An excellent model to study coordinated cell movements is provided by the migration of border cell clusters within a developing Drosophila egg chamber. In a mutagenesis screen, we isolated two alleles of the gene rickets (rk) encoding a G-protein-coupled receptor. The rk alleles result in border cell migration defects in a significant fraction of egg chambers. In rk mutants, border cells are properly specified and express the marker Slbo. Yet, analysis of both fixed as well as live samples revealed that some single border cells lag behind the main border cell cluster during migration, or, in other cases, the entire border cell cluster can remain tethered to the anterior epithelium as it migrates...
June 15, 2016: Developmental Biology
George Aranjuez, Ashley Burtscher, Ketki Sawant, Pralay Majumder, Jocelyn A McDonald
Migrating cells need to overcome physical constraints from the local microenvironment to navigate their way through tissues. Cells that move collectively have the additional challenge of negotiating complex environments in vivo while maintaining cohesion of the group as a whole. The mechanisms by which collectives maintain a migratory morphology while resisting physical constraints from the surrounding tissue are poorly understood. Drosophila border cells represent a genetic model of collective migration within a cell-dense tissue...
June 15, 2016: Molecular Biology of the Cell
Kenneth A Halberg, Stephanie M Rainey, Iben R Veland, Helen Neuert, Anthony J Dornan, Christian Klämbt, Shireen-Anne Davies, Julian A T Dow
Multicellular organisms rely on cell adhesion molecules to coordinate cell-cell interactions, and to provide navigational cues during tissue formation. In Drosophila, Fasciclin 2 (Fas2) has been intensively studied due to its role in nervous system development and maintenance; yet, Fas2 is most abundantly expressed in the adult renal (Malpighian) tubule rather than in neuronal tissues. The role Fas2 serves in this epithelium is unknown. Here we show that Fas2 is essential to brush border maintenance in renal tubules of Drosophila...
2016: Nature Communications
Chih-Wen Chu, Olga Ossipova, Andriani Ioannou, Sergei Y Sokol
PCP proteins maintain planar polarity in many epithelial tissues and have been implicated in cilia development in vertebrate embryos. In this study we examine Prickle3 (Pk3), a vertebrate homologue of Drosophila Prickle, in Xenopus gastrocoel roof plate (GRP). GRP is a tissue equivalent to the mouse node, in which cilia-generated flow promotes left-right patterning. We show that Pk3 is enriched at the basal body of GRP cells but is recruited by Vangl2 to anterior cell borders. Interference with Pk3 function disrupted the anterior polarization of endogenous Vangl2 and the posterior localization of cilia in GRP cells, demonstrating its role in PCP...
2016: Scientific Reports
Brian A Camley, Juliane Zimmermann, Herbert Levine, Wouter-Jan Rappel
Many eukaryotic cells chemotax, sensing and following chemical gradients. However, experiments show that even under conditions when single cells cannot chemotax, small clusters may still follow a gradient. This behavior is observed in neural crest cells, in lymphocytes, and during border cell migration in Drosophila, but its origin remains puzzling. Here, we propose a new mechanism underlying this "collective guidance," and study a model based on this mechanism both analytically and computationally. Our approach posits that contact inhibition of locomotion, where cells polarize away from cell-cell contact, is regulated by the chemoattractant...
March 4, 2016: Physical Review Letters
Christopher R Schlieve, Salvador Garcia Mojica, Kathleen A Holoyda, Xiaogang Hou, Kathryn L Fowler, Tracy C Grikscheit
BACKGROUND: Vascular endothelial growth factor (VEGF) is a highly conserved, master regulatory molecule required for endothelial cell proliferation, organization, migration and branching morphogenesis. Podocoryne carnea and drosophila, which lack endothelial cells and a vascular system, express VEGF homologs, indicating potential roles beyond angiogenesis and vasculogenesis. The role of VEGF in the development and homeostasis of the postnatal small intestine is unknown. We hypothesized regulating VEGF bioavailability in the postnatal small intestine would exhibit effects beyond the vasculature and influence epithelial cell stem/progenitor populations...
2016: PloS One
Mariam H Orme, Gianmaria Liccardi, Nina Moderau, Rebecca Feltham, Sidonie Wicky-John, Tencho Tenev, Lior Aram, Rebecca Wilson, Katiuscia Bianchi, Otto Morris, Celia Monteiro Domingues, David Robertson, Meghana Tare, Alexander Wepf, David Williams, Andreas Bergmann, Matthias Gstaiger, Eli Arama, Paulo S Ribeiro, Pascal Meier
Caspases provide vital links in non-apoptotic regulatory networks controlling inflammation, compensatory proliferation, morphology and cell migration. How caspases are activated under non-apoptotic conditions and process a selective set of substrates without killing the cell remain enigmatic. Here we find that the Drosophila unconventional myosin CRINKLED (CK) selectively interacts with the initiator caspase DRONC and regulates some of its non-apoptotic functions. Loss of CK in the arista, border cells or proneural clusters of the wing imaginal discs affects DRONC-dependent patterning...
March 10, 2016: Nature Communications
Wenjuan Xiang, Dabing Zhang, Denise J Montell
Collective cell migration is emerging as a major contributor to normal development and disease. Collective movement of border cells in the Drosophila ovary requires cooperation between two distinct cell types: four to six migratory cells surrounding two immotile cells called polar cells. Polar cells secrete a cytokine, Unpaired (Upd), which activates JAK/STAT signaling in neighboring cells, stimulating their motility. Without Upd, migration fails, causing sterility. Ectopic Upd expression is sufficient to stimulate motility in otherwise immobile cells...
January 1, 2016: Molecular Biology of the Cell
Prashanth R Rao, Li Lin, Hai Huang, Arjun Guha, Sougata Roy, Thomas B Kornberg
The Drosophila tracheal system is a branched tubular network that forms in the embryo by a post-mitotic program of morphogenesis. In third instar larvae (L3), cells constituting the second tracheal metamere (Tr2) reenter the cell cycle. Clonal analysis of L3 Tr2 revealed that dividing cells in the dorsal trunk, dorsal branch and transverse connective branches respect lineage restriction boundaries near branch junctions. These boundaries corresponded to domains of gene expression, for example where cells expressing Spalt, Delta and Serrate in the dorsal trunk meet vein-expressing cells in the dorsal branch or transverse connective...
October 22, 2015: ELife
Martina Felix, Mrinal Chayengia, Ritabrata Ghosh, Aditi Sharma, Mohit Prasad
Group cell migration is a highly coordinated process that is involved in a number of physiological events such as morphogenesis, wound healing and tumor metastasis. Unlike single cells, collectively moving cells are physically attached to each other and retain some degree of apical-basal polarity during the migratory phase. Although much is known about direction sensing, how polarity is regulated in multicellular movement remains unclear. Here we report the role of the protein kinase Pak3 in maintaining apical-basal polarity in migrating border cell clusters during Drosophila oogenesis...
November 1, 2015: Development
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