Bi-directional gap junction-mediated Soma-Germline communication is essential for spermatogenesis

Smendziuk, Christopher M.; Messenberg, Anat; Vogl, A. Wayne; Tanentzapf, Guy

doi:10.1242/dev.123448

Cited by 42 publications

(59 citation statements)

References 55 publications

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“…As germ line clones for Inx2 didn’t influence BC fate, it is likely that Inx2 plays a significant role only in the follicle cells where as another germ line specific gap junction family protein may partner with Inx2. Interestingly, gap junction mediated germline-soma interaction of this nature has been reported in Drosophila spermatogenesis [41]. In this instance, Inx2 from the somatic cells and Inx4 from male germ line form a heterotypic channel critical for mediating effective germline-soma communication during spermatogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…The following primary antibodies were used: mouse anti-Armadillo [Developmental Studies Hybridoma Bank (DSHB), 1:25, N27A1]; rat anti-Slbo 1:400 (gift from P. Rorth); rabbit anti-STAT 1:700 (gift from Steven Hou), rabbit anti-GFP 1:1000 (Life technologies), guinea pig anti-Inx2 1:1000 [41] and mouse anti-Dynamin 1:500 (BD, gift from Dr Richa Rikhy). Secondary antibodies conjugated with Alexa-488 and Alexa-568 (Molecular Probes) were used at 1:250 and 1:400 dilutions respectively.…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2017

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Intercellular communication mediated by gap junction (GJ) proteins is indispensable during embryogenesis, tissue regeneration and wound healing. Here we report functional analysis of a gap junction protein, Innexin 2 (Inx2), in cell type specification during Drosophila oogenesis. Our data reveal a novel involvement of Inx2 in the specification of Border Cells (BCs), a migratory cell type, whose identity is determined by the cell autonomous STAT activity. We show that Inx2 influences BC fate specification by modulating STAT activity via Domeless receptor endocytosis. Furthermore, detailed experimental analysis has uncovered that Inx2 also regulates a calcium flux that transmits across the follicle cells. We propose that Inx2 mediated calcium flux in the follicle cells stimulates endocytosis by altering Dynamin (Shibire) distribution which is in turn critical for careful calibration of STAT activation and, thus for BC specification. Together our data provide unprecedented molecular insights into how gap junction proteins can regulate cell-type specification.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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

et al. 2017

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“…Germ line stem cells differentiate upon losing contact with their niche, which likely involves GJC; as an example, it has been proposed that GJ‐mediated cAMP signaling between blastomeres and somatic cells results in changes in somatic cell gene expression (Burnside and Collas, ). Many instances of GJC‐dependent regulation is bidirectional, with several cell types exchanging instructive information, such as occurs in the communication between stem cells and their neighbors in spermatogenesis during germline differentiation (Smendziuk et al, ).…”

Section: Gjs In Cellular Regulationmentioning

confidence: 99%

Gap junctional signaling in pattern regulation: Physiological network connectivity instructs growth and form

Mathews

Levin

2016

Developmental Neurobiology

121

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Gap junctions (GJs) are aqueous channels that allow cells to communicate via physiological signals directly. The role of gap junctional connectivity in determining single-cell functions has long been recognized. However, GJs have another important role: the regulation of large-scale anatomical pattern. GJs are not only versatile computational elements that allow cells to control which small molecule signals they receive and emit, but also establish connectivity patterns within large groups of cells. By dynamically regulating the topology of bioelectric networks in vivo, GJs underlie the ability of many tissues to implement complex morphogenesis. Here, a review of recent data on patterning roles of GJs in growth of the zebrafish fin, the establishment of left-right patterning, the developmental dysregulation known as cancer, and the control of large-scale head-tail polarity, and head shape in planarian regeneration has been reported. A perspective in which GJs are not only molecular features functioning in single cells, but also enable global neural-like dynamics in non-neural somatic tissues has been proposed. This view suggests a rich program of future work which capitalizes on the rapid advances in the biophysics of GJs to exploit GJ-mediated global dynamics for applications in birth defects, regenerative medicine, and morphogenetic bioengineering. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 643-673, 2017.

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“…Microinjected antibodies directed against presumed cytoplasmic regions of Inx2 specifically blocked intercellular communication and lead to inhibitory effects on oogenesis that were similar to those obtained with antibodies directed against presumed cytoplasmic regions of ductin [ 18 ]. Even during spermatogenesis, Inx2 was found to be involved in soma-to-germ line intercellular communication [ 51 ]. Moreover, it has been demonstrated that, within the germarium, Inx2 supports germ-cell survival, cyst formation and early follicle development [ 52 ].…”

Section: Discussionmentioning

confidence: 99%

Relating proton pumps with gap junctions: colocalization of ductin, the channel-forming subunit c of V-ATPase, with subunit a and with innexins 2 and 3 during Drosophila oogenesis

Lautemann

Bohrmann

2016

BMC Dev Biol

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BackgroundIon-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. We, therefore, investigated the stage-specific distribution patterns of V-ATPase components in relation to gap-junction proteins.ResultsWe analysed the localization of the V-ATPase components ductin (subunit c) and subunit a, and the gap-junction components innexins 2 and 3, especially in polar cells, border cells, stalk cells and centripetally migrating cells. These types of follicle cells had previously been shown to exhibit characteristic patterns of membrane channels as well as membrane potential and intracellular pH. Stage-specifically, ductin and subunit a were found either colocalized or separately enriched in different regions of soma and germ-line cells. While ductin was often more prominent in plasma membranes, subunit a was more prominent in cytoplasmic and nuclear vesicles. Particularly, ductin was enriched in polar cells, stalk cells, and nurse-cell membranes, whereas subunit a was enriched in the cytoplasm of border cells, columnar follicle cells and germ-line cells. Comparably, ductin and both innexins 2 and 3 were either colocalized or separately enriched in different cellular regions. While ductin often showed a continuous membrane distribution, the distribution of both innexins was mostly punctate. Particularly, ductin was enriched in polar cells and stalk cells, whereas innexin 2 was enriched in the oolemma, and innexin 3 in centripetally migrating follicle cells. In lateral follicle-cell membranes, the three proteins were found colocalized as well as separately concentrated in presumed gap-junction plaques.ConclusionsOur results support the notion of a large variety of gap junctions existing in the Drosophila ovary. Moreover, since ductin is the channel-forming part of a proton pump and, like the innexins, is able to form junctional as well as non-junctional membrane channels, a plethora of cellular functions could be realized by using these proteins. The distribution and activity patterns of such membrane channels are expected to contribute to developmentally important bioelectric signals.

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Bi-directional gap junction-mediated Soma-Germline communication is essential for spermatogenesis

Cited by 42 publications

References 55 publications

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

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

Gap junctional signaling in pattern regulation: Physiological network connectivity instructs growth and form

Relating proton pumps with gap junctions: colocalization of ductin, the channel-forming subunit c of V-ATPase, with subunit a and with innexins 2 and 3 during Drosophila oogenesis

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