A Gap Junction Protein, Inx2, Modulates Calcium Flux to Specify Border Cell Fate during Drosophila oogenesis

Sahu, Aresh; Ghosh, Ritabrata; Deshpande, Girish; Prasad, Mohit

doi:10.1371/journal.pgen.1006542

“…We highlighted 14 representative genes involved in epithelial development (GO: 0060429, P adj = 1.101e −5 ), the highly enriched GO term in this cluster. These include markers for border cell migration, such as sn, jar, and Inx2 [15,[87][88][89]. We also detected in this cluster the expression of Cad99C, which has been reported in several MBFCs and anterior-migrating centripetal cells [83].…”

Section: Expression Profiles Of Migrating Border and Centripetal Cellssupporting

confidence: 69%

A single-cell atlas of adult Drosophila ovary identifies transcriptional programs and somatic cell lineage regulating oogenesis

Jevitt

¹

,

Chatterjee

²

,

Xie

³

et al. 2020

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Oogenesis is a complex developmental process that involves spatiotemporally regulated coordination between the germline and supporting, somatic cell populations. This process has been modeled extensively using the Drosophila ovary. Although different ovarian cell types have been identified through traditional means, the large-scale expression profiles underlying each cell type remain unknown. Using single-cell RNA sequencing technology, we have built a transcriptomic data set for the adult Drosophila ovary and connected tissues. Using this data set, we identified the transcriptional trajectory of the entire follicle-cell population over the course of their development from stem cells to the oogenesis-to-ovulation transition. We further identify expression patterns during essential developmental events that take place in somatic and germline cell types such as differentiation, cell-cycle switching, migration, symmetry breaking, nurse-cell engulfment, eggshell formation, and corpus luteum signaling. Extensive experimental validation of unique expression patterns in both ovarian and nearby, nonovarian cells also led to the identification of many new cell type-and stage-specific markers. The inclusion of several nearby tissue types in this data set also led to our identification of functional convergence in expression between distantly related cell types such as the immune-related genes that were similarly expressed in immune cells (hemocytes) and ovarian somatic cells (stretched cells) during their brief phagocytic role in nurse-cell engulfment. Taken together, these findings provide new insight into the temporal regulation of genes in a cell-type specific manner during oogenesis and begin to reveal the relatedness in expression between cell and tissues types.

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“…We highlighted 14 representative genes involved in epithelial development (GO : 0060429, P adj = 1.101e −5 ), the highly enriched GO term in this cluster. These include markers for border cell migration, such as sn, jar, and Inx2 [25,35,45,79]. We also detected in this cluster the expression of Cad99C, which has been reported in several main body follicle cells, and anterior-migrating centripetal cells [21].…”

Section: Expression Profiles Of Migrating Border and Centripetal Cellssupporting

confidence: 69%

Single-cell RNA sequencing of adultDrosophilaovary identifies transcriptional programs governing oogenesis

Jevitt¹,

Chatterjee²,

Xie³

et al. 2019

Preprint

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Oogenesis is a complex developmental process that involves spatiotemporally regulated coordination between the germline and supporting, somatic cell populations. This process has been modelled extensively using the Drosophila ovary. While different ovarian cell types have been identified through traditional means, the large-scale expression profiles underlying each cell type remain unknown. Using single-cell RNA sequencing technology, we have built a transcriptomic dataset for the adult Drosophila ovary and connected tissues. This dataset captures the entire transcriptional trajectory of the developing follicle cell population over time. Our findings provide detailed insight into processes such as cell-cycle switching, migration, symmetry breaking, nurse cell engulfment, egg-shell formation, and signaling during corpus luteum formation, marking a newly identified oogenesis-to-ovulation transition. Altogether, these findings provide a broad perspective on oogenesis at a single-cell resolution while revealing new genetic markers and fate-specific transcriptional signatures to facilitate future studies.

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“…We therefore conclude that the gap junction channels composed of INX5 in αβ neurons are critical for ARM retrieval (Fig 7). A recent study showed that the gap junction protein INX2 regulates calcium transmission across the follicle cells during Drosophila oogenesis[37]. In addition, INX1/INX2 induces calcium oscillations in the glial cells of the blood-brain barrier (BBB), enabling signal amplification and synchronization across the BBB in fruit flies[26].…”

Section: Discussionmentioning

confidence: 99%

Electrical synapses between mushroom body neurons are critical for consolidated memory retrieval in Drosophila

Shyu¹,

Lee²,

Chiang³

et al. 2019

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Electrical synapses between neurons, also known as gap junctions, are direct cell membrane channels between adjacent neurons. Gap junctions play a role in the synchronization of neuronal network activity; however, their involvement in cognition has not been well characterized. Three-hour olfactory associative memory in Drosophila has two components: consolidated anesthesia-resistant memory (ARM) and labile anesthesia-sensitive memory (ASM). Here, we show that knockdown of the gap junction gene innexin5 (inx5) in mushroom body (MB) neurons disrupted ARM, while leaving ASM intact. Whole-mount brain immunohistochemistry indicated that INX5 protein was preferentially expressed in the somas, calyxes, and lobes regions of the MB neurons. Adult-stage-specific knockdown of inx5 in αβ neurons disrupted ARM, suggesting a specific requirement of INX5 in αβ neurons for ARM formation. Hyperpolarization of αβ neurons during memory retrieval by expressing an engineered halorhodopsin (eNpHR) also disrupted ARM. Administration of the gap junction blocker carbenoxolone (CBX) reduced the proportion of odor responsive αβ neurons to the training odor 3 hours after training. Finally, the α-branch-specific 3-hour ARM-specific memory trace was also diminished with CBX treatment and in inx5 knockdown flies. Altogether, our results suggest INX5 gap junction channels in αβ neurons for ARM retrieval and also provide a more detailed neuronal mechanism for consolidated memory in Drosophila .

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A Gap Junction Protein, Inx2, Modulates Calcium Flux to Specify Border Cell Fate during Drosophila oogenesis

Cited by 23 publications

References 50 publications

A single-cell atlas of adult Drosophila ovary identifies transcriptional programs and somatic cell lineage regulating oogenesis

A single-cell atlas of adult Drosophila ovary identifies transcriptional programs and somatic cell lineage regulating oogenesis

Single-cell RNA sequencing of adultDrosophilaovary identifies transcriptional programs governing oogenesis

Electrical synapses between mushroom body neurons are critical for consolidated memory retrieval in Drosophila

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