Quantitative Image Analysis of Dynamic Cell Behaviors During Border Cell Migration

Chen, Yujun; Kotian, Nirupama; McDonald, Jocelyn A.

doi:10.1007/978-1-0716-2970-3_10

Cited by 4 publications

(3 citation statements)

References 39 publications

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“…To isolate staged egg chambers for cell sorting, whole ovaries were first dissected from fattened 3- to 5-day old slbo- mCD8:GFP/+ females followed by dissection into ovarioles in room temperature “live imaging media” [Schneider’s media, pH 6.95 (Thermo Fisher Scientific),15% fetal bovine serum [Seradigm FBS; FBS (VWR), 200 µg/mL insulin (bovine pancreatic, Sigma-Millipore #I5500)] [97]. Stages 9 and 10 egg chambers [13] were manually selected in a two-well concave slide by observing GFP in the border cells ( slbo- mCD8:GFP) on a fluorescent stereomicroscope.…”

Section: Methodsmentioning

confidence: 99%

Transcriptome analysis reveals temporally regulated genetic networks duringDrosophilaborder cell collective migration

Burghardt,

Rakijas,

Tyagi

et al. 2023

Preprint

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BackgroundCollective cell migration underlies many essential processes, including sculpting organs during embryogenesis, wound healing in the adult, and metastasis of cancer cells. At mid-oogenesis,Drosophilaborder cells undergo collective migration. Border cells round up into a small group, detach from the epithelium, and migrate – at first rapidly through the surrounding tissue, then slower, with the cluster rotating several times before stopping at the oocyte. While specific genes that promote cell signaling, polarization of the cluster, formation of protrusions, and cell-cell adhesion are known to regulate border cell migration, there may be additional genes that promote these distinct dynamic phases of border cell migration. Therefore, we sought to identify genes whose expression patterns changed during border cell migration.ResultsWe performed RNA-sequencing on border cells isolated at pre-, mid-, and late-migration stages. We report that 1,729 transcripts, in nine co-expression gene clusters, are temporally and differentially expressed across the three migration stages. Gene ontology analyses and constructed protein-protein interaction networks identified genes expected to function in collective migration, such as regulators of the cytoskeleton, adhesion, and tissue morphogenesis, but also a notable enrichment of genes involved in immune signaling, ribosome biogenesis, and stress responses. Finally, we validated thein vivoexpression and function of a subset of identified genes in border cells.ConclusionsOverall, our results identified differentially and temporally expressed genetic networks that may facilitate the efficient development and migration of border cells. The genes identified here represent a wealth of new candidates to investigate the molecular nature of dynamic collective cell migrations in developing tissues.

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Section: Methodsmentioning

confidence: 99%

Transcriptome analysis reveals temporally regulated genetic networks duringDrosophilaborder cell collective migration

Burghardt,

Rakijas,

Tyagi

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…no. I5500)] [ 99 ]. Stages 9 and 10 egg chambers [ 14 ] were manually selected in a two-well concave slide by observing GFP in the border cells ( slbo- mCD8:GFP) on a fluorescence stereomicroscope.…”

Section: Methodsmentioning

confidence: 99%

Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration

Burghardt,

Rakijas,

Tyagi

et al. 2023

BMC Genomics

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Background Collective cell migration underlies many essential processes, including sculpting organs during embryogenesis, wound healing in the adult, and metastasis of cancer cells. At mid-oogenesis, Drosophila border cells undergo collective migration. Border cells round up into a small group at the pre-migration stage, detach from the epithelium and undergo a dynamic and highly regulated migration at the mid-migration stage, and stop at the oocyte, their final destination, at the post-migration stage. While specific genes that promote cell signaling, polarization of the cluster, formation of protrusions, and cell-cell adhesion are known to regulate border cell migration, there may be additional genes that promote these distinct active phases of border cell migration. Therefore, we sought to identify genes whose expression patterns changed during border cell migration. Results We performed RNA-sequencing on border cells isolated at pre-, mid-, and post-migration stages. We report that 1,729 transcripts, in nine co-expression gene clusters, are temporally and differentially expressed across the three migration stages. Gene ontology analyses and constructed protein-protein interaction networks identified genes expected to function in collective migration, such as regulators of the cytoskeleton, adhesion, and tissue morphogenesis, but also uncovered a notable enrichment of genes involved in immune signaling, ribosome biogenesis, and stress responses. Finally, we validated the in vivo expression and function of a subset of identified genes in border cells. Conclusions Overall, our results identified differentially and temporally expressed genetic networks that may facilitate the efficient development and migration of border cells. The genes identified here represent a wealth of new candidates to investigate the molecular nature of dynamic collective cell migrations in developing tissues.

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“…All data needed to evaluate the conclusions in the paper are present in the paper and supporting information [SRA ID: PRJNA921886 ( 51 ) (RNA-seq and analyzed data)].…”

Section: Data Materials and Software Availabilitymentioning

confidence: 99%

The Drosophila NPY-like system protects against chronic stress–induced learning deficit by preventing the disruption of autophagic flux

Chen,

Zhang,

Ding

et al. 2023

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

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Chronic stress may induce learning and memory deficits that are associated with a depression-like state in Drosophila melanogaster . The molecular and neural mechanisms underlying the etiology of chronic stress–induced learning deficit (CSLD) remain elusive. Here, we show that the autophagy-lysosomal pathway, a conserved cellular signaling mechanism, is associated with chronic stress in Drosophila , as indicated by time-series transcriptome profiling. Our findings demonstrate that chronic stress induces the disruption of autophagic flux, and chronic disruption of autophagic flux could lead to a learning deficit. Remarkably, preventing the disruption of autophagic flux by up-regulating the basal autophagy level is sufficient to protect against CSLD. Consistent with the essential role of the dopaminergic system in modulating susceptibility to CSLD, dopamine neuronal activity is also indispensable for chronic stress to induce the disruption of autophagic flux. By screening knockout mutants, we found that neuropeptide F, the Drosophila homolog of neuropeptide Y, is necessary for normal autophagic flux and promotes resilience to CSLD. Moreover, neuropeptide F signaling during chronic stress treatment promotes resilience to CSLD by preventing the disruption of autophagic flux. Importantly, neuropeptide F receptor activity in dopamine neurons also promotes resilience to CSLD. Together, our data elucidate a mechanism by which stress-induced excessive dopaminergic activity precipitates the disruption of autophagic flux, and chronic disruption of autophagic flux leads to CSLD, while inhibitory neuropeptide F signaling to dopamine neurons promotes resilience to CSLD by preventing the disruption of autophagic flux.

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Quantitative Image Analysis of Dynamic Cell Behaviors During Border Cell Migration

Cited by 4 publications

References 39 publications

Transcriptome analysis reveals temporally regulated genetic networks duringDrosophilaborder cell collective migration

Transcriptome analysis reveals temporally regulated genetic networks duringDrosophilaborder cell collective migration

Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration

The Drosophila NPY-like system protects against chronic stress–induced learning deficit by preventing the disruption of autophagic flux

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