Cellular and Molecular Mechanisms of Border Cell Migration Analyzed Using Time-Lapse Live-Cell Imaging

Prasad, Mohit; Montell, Denise J.

doi:10.1016/j.devcel.2007.03.021

Cited by 222 publications

(293 citation statements)

References 41 publications

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“…SlboGal4, UAS-dsRedNLS; UASmoesinGFP, and slbo-Lifeact-GFP flies were used for live imaging and were described before (26,29). UAS-PVR DN , UAS-EGFR DN , and UAS-EcadRNAi (VDRC: KK103962) were described previously (23,24,26,29).…”

Section: Methodsmentioning

confidence: 99%

“…During migration, the cells respond to at least four secreted factors produced in the germ line: PDGF-and VEGF-related factor 1 (PVF1), which binds to and activates its receptor (PVR), as well as Spitz, Keren, and Gurken (Grk), which bind and activate epidermal growth factor receptor (EGFR), which like PVR is a receptor tyrosine kinase. Inhibiting both receptors in the border cells at the same time causes the cells to migrate poorly and sometimes off-track (23)(24)(25)(26). It would be interesting to directly measure the spatial profiles of the ligands; however, antibodies are only available against PVF1 and Grk, and the extracellular protein is not abundant enough to detect.…”

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confidence: 99%

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Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Cai

Dai

Prasad

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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A long-standing question in collective cell migration has been what might be the relative advantage of forming a cluster over migrating individually. Does an increase in the size of a collectively migrating group of cells enable them to sample the chemical gradient over a greater distance because the difference between front and rear of a cluster would be greater than for single cells? We combined theoretical modeling with experiments to study collective migration of the border cells in-between nurse cells in the Drosophila egg chamber. We discovered that cluster size is positively correlated with migration speed, up to a particular point above which speed plummets. This may be due to the effect of viscous drag from surrounding nurse cells together with confinement of all of the cells within a stiff extracellular matrix. The model predicts no relationship between cluster size and velocity for cells moving on a flat surface, in contrast to movement within a 3D environment. Our analyses also suggest that the overall chemoattractant profile in the egg chamber is likely to be exponential, with the highest concentration in the oocyte. These findings provide insights into collective chemotaxis by combining theoretical modeling with experimentation.cell migration | theoretical modeling | three-dimensional | chemotaxis

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Cai

Dai

Prasad

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…This attachment provides an inherent polarity for each cell, as intracluster cell interactions are distinguishable from interactions with the nurse-cell substrate. Live imaging has shown border cell migration to be very dynamic, with cells exchanging places frequently (9,10). Border cells are directed by guidance cues from the oocyte and use two RTKs (PVR and EGFR) to read these cues (12,13).…”

mentioning

confidence: 99%

“…The system is genetically tractable and allows live imaging in the tissue, making it a good model for studying collective cell migration (9,10). Once specified, border cells delaminate from the follicular epithelium, invade the underlying germ line tissue, and migrate between the giant nurse cells to the oocyte.…”

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confidence: 99%

Direct detection of guidance receptor activity during border cell migration

Janssens

Sung

Rørth

2010

Proc. Natl. Acad. Sci. U.S.A.

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Guidance receptor signaling is crucial for steering migrating cells. Despite this, we generally lack direct measurements of such signaling. Border cells in Drosophila migrate as a tightly associated group, but dynamically, with front and rear cells exchanging places. They use the receptor tyrosine kinase (RTK) PDGF/VEGF receptor (PVR) as a guidance receptor, perceiving the attractant Pvf1. Here we determine the spatial distribution of PVR signaling by generating an antibody that specifically detects activated PVR in situ. PVR activity is very low in migrating border cells, due to strong activity of cellular phosphatases. Measurements of signal at the cell cortex show variability but a strong bias for both total active PVR and specific activity of PVR to be elevated at the front versus side of the leading cell, often with several-fold difference in signal levels. This polarized active PVR signal requires the E3 ubiquitin ligase Cbl and the recycling regulator Rab11, indicating a dependency on receptor trafficking. The endogenous ligand gradient contributes to shaping of signaling by increasing the specific activity of PVR toward the source in front cells. Surprisingly, signaling is also elevated at the back versus the side of rear cells. This distally polarized distribution of active PVR is ligand independent. Thus the actual guidance signal transmitted in border cells appears to integrate perceived ligand distribution with cell polarity or cell orientation with respect to the cluster. A general implication is that both group configuration and extrinsic cues can directly modulate guidance receptor signaling during collective cell migration.

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“…As these organisms are thinner and smaller than mammals and also relatively easy to manipulate, better resolution can be achieved with spinning-disc or conventional confocal microscopy. Recent studies of border and immune cells in Drosophila, and neurons in zebrafish have revealed exciting new information regarding cell migration and adhesion within intact organisms and the signalling mechanisms responsible for driving these events (Bianco et al, 2007;Koster and Fraser, 2001;Prasad and Montell, 2007;Robles and Gomez, 2006;Stramer et al, 2005).…”

Section: Visualising Adhesions In Whole Organismsmentioning

confidence: 99%

Advances in imaging cell–matrix adhesions

Worth

Parsons

2010

Journal of Cell Science

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SummaryAdhesion is fundamental to the survival and function of many different cell types, and regulates basic events such as mitosis, cell survival and migration, in both embryonic and adult organisms. Cell-matrix adhesion also regulates the dynamic interplay between cells and surrounding tissues during processes such as immune cell recruitment, wound healing and cancer cell metastasis. The study of cell adhesion has gained momentum in recent years, in large part because of the emergence of imaging techniques that have facilitated detailed analysis of the molecular composition and dynamics of the structures involved. In this Commentary, we discuss the recent application of different imaging techniques to study cell-matrix adhesions, emphasising common strategies used for the analysis of adhesion dynamics both in cells in culture and in whole organisms.

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Cellular and Molecular Mechanisms of Border Cell Migration Analyzed Using Time-Lapse Live-Cell Imaging

Cited by 222 publications

References 41 publications

Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Direct detection of guidance receptor activity during border cell migration

Advances in imaging cell–matrix adhesions

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