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Bioelectric patterning during oogenesis: stage-specific distribution of membrane potentials, intracellular pH and ion-transport mechanisms in Drosophila ovarian follicles.

Krüger J, Bohrmann J - BMC Dev. Biol. (2015)

Bottom Line: Bioelectric phenomena have been found to exert influence on various developmental and regenerative processes.Striking similarities between Vmem-patterns and activity patterns of voltage-dependent Ca(2+)-channels were found, suggesting a mechanism for transducing bioelectric signals into cellular responses.Our data suggest that spatial patterning of Vmem, pHi and specific membrane-channel proteins results in bioelectric signals that are supposed to play important roles during oogenesis, e. g. by influencing spatial coordinates, regulating migration processes or modifying the cytoskeletal organization.

View Article: PubMed Central - PubMed

Affiliation: RWTH Aachen University, Institut für Biologie II, Abt. Zoologie und Humanbiologie, Worringerweg 3, 52056, Aachen, Germany. Julia-Krueger@gmx.net.

ABSTRACT

Background: Bioelectric phenomena have been found to exert influence on various developmental and regenerative processes. Little is known about their possible functions and the cellular mechanisms by which they might act during Drosophila oogenesis. In developing follicles, characteristic extracellular current patterns and membrane-potential changes in oocyte and nurse cells have been observed that partly depend on the exchange of protons, potassium ions and sodium ions. These bioelectric properties have been supposed to be related to various processes during oogenesis, e. g. pH-regulation, osmoregulation, cell communication, cell migration, cell proliferation, cell death, vitellogenesis and follicle growth. Analysing in detail the spatial distribution and activity of the relevant ion-transport mechanisms is expected to elucidate the roles that bioelectric phenomena play during oogenesis.

Results: To obtain an overview of bioelectric patterning along the longitudinal and transversal axes of the developing follicle, the spatial distributions of membrane potentials (Vmem), intracellular pH (pHi) and various membrane-channel proteins were studied systematically using fluorescent indicators, fluorescent inhibitors and antisera. During mid-vitellogenic stages 9 to 10B, characteristic, stage-specific Vmem-patterns in the follicle-cell epithelium as well as anteroposterior pHi-gradients in follicle cells and nurse cells were observed. Corresponding distribution patterns of proton pumps (V-ATPases), voltage-dependent L-type Ca(2+)-channels, amiloride-sensitive Na(+)-channels and Na(+),H(+)-exchangers (NHE) and gap-junction proteins (innexin 3) were detected. In particular, six morphologically distinguishable follicle-cell types are characterized on the bioelectric level by differences concerning Vmem and pHi as well as specific compositions of ion channels and carriers. Striking similarities between Vmem-patterns and activity patterns of voltage-dependent Ca(2+)-channels were found, suggesting a mechanism for transducing bioelectric signals into cellular responses. Moreover, gradients of electrical potential and pH were observed within single cells.

Conclusions: Our data suggest that spatial patterning of Vmem, pHi and specific membrane-channel proteins results in bioelectric signals that are supposed to play important roles during oogenesis, e. g. by influencing spatial coordinates, regulating migration processes or modifying the cytoskeletal organization. Characteristic stage-specific changes of bioelectric activity in specialized cell types are correlated with various developmental processes.

No MeSH data available.


Six follicle-cell types are distinguishable on the morphological and on the molecular level. Schematic drawing, S10B. Each population is indicated by a different colour and consists of multiple cells which are not shown in detail, except for the polar cells (2 cells) and the border cells (6–10 cells). Anterior is to the left. The position of the oocyte nucleus (black) marks the dorsal side. BC: border cells, cFC: centripetal follicle cells, mFC: mainbody follicle cells, NC: nurse cells, Ooc: oocyte, PC: polar cells, sFC: stretched follicle cells, tFC: terminal follicle cells.
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Fig1: Six follicle-cell types are distinguishable on the morphological and on the molecular level. Schematic drawing, S10B. Each population is indicated by a different colour and consists of multiple cells which are not shown in detail, except for the polar cells (2 cells) and the border cells (6–10 cells). Anterior is to the left. The position of the oocyte nucleus (black) marks the dorsal side. BC: border cells, cFC: centripetal follicle cells, mFC: mainbody follicle cells, NC: nurse cells, Ooc: oocyte, PC: polar cells, sFC: stretched follicle cells, tFC: terminal follicle cells.

Mentions: According to morphological criteria, Drosophila oogenesis has been divided into 14 stages (S1 to S14). In the FC epithelium, 6 types of cells can be distinguished on the morphological as well as on the molecular level during mid-vitellogenic stages 9 to 10B [14-16] (Figure 1). The terminal FC (tFC) are a population of about 200 cells at the posterior follicle pole. The mainbody FC (mFC) form a broad band anterior to the tFC. The centripetal FC (cFC) reside at the anterior end of the Ooc and migrate in between NC and Ooc during S10B. The stretched FC (sFC) become flattened and cover the NC. A pair of polar cells (PC) resides at the posterior pole of the Ooc. The border cells (BC), a group of 6–10 anterior FC, migrate between the NC from the anterior follicle pole to the anterior pole of the Ooc during S9.Figure 1


Bioelectric patterning during oogenesis: stage-specific distribution of membrane potentials, intracellular pH and ion-transport mechanisms in Drosophila ovarian follicles.

Krüger J, Bohrmann J - BMC Dev. Biol. (2015)

Six follicle-cell types are distinguishable on the morphological and on the molecular level. Schematic drawing, S10B. Each population is indicated by a different colour and consists of multiple cells which are not shown in detail, except for the polar cells (2 cells) and the border cells (6–10 cells). Anterior is to the left. The position of the oocyte nucleus (black) marks the dorsal side. BC: border cells, cFC: centripetal follicle cells, mFC: mainbody follicle cells, NC: nurse cells, Ooc: oocyte, PC: polar cells, sFC: stretched follicle cells, tFC: terminal follicle cells.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4302609&req=5

Fig1: Six follicle-cell types are distinguishable on the morphological and on the molecular level. Schematic drawing, S10B. Each population is indicated by a different colour and consists of multiple cells which are not shown in detail, except for the polar cells (2 cells) and the border cells (6–10 cells). Anterior is to the left. The position of the oocyte nucleus (black) marks the dorsal side. BC: border cells, cFC: centripetal follicle cells, mFC: mainbody follicle cells, NC: nurse cells, Ooc: oocyte, PC: polar cells, sFC: stretched follicle cells, tFC: terminal follicle cells.
Mentions: According to morphological criteria, Drosophila oogenesis has been divided into 14 stages (S1 to S14). In the FC epithelium, 6 types of cells can be distinguished on the morphological as well as on the molecular level during mid-vitellogenic stages 9 to 10B [14-16] (Figure 1). The terminal FC (tFC) are a population of about 200 cells at the posterior follicle pole. The mainbody FC (mFC) form a broad band anterior to the tFC. The centripetal FC (cFC) reside at the anterior end of the Ooc and migrate in between NC and Ooc during S10B. The stretched FC (sFC) become flattened and cover the NC. A pair of polar cells (PC) resides at the posterior pole of the Ooc. The border cells (BC), a group of 6–10 anterior FC, migrate between the NC from the anterior follicle pole to the anterior pole of the Ooc during S9.Figure 1

Bottom Line: Bioelectric phenomena have been found to exert influence on various developmental and regenerative processes.Striking similarities between Vmem-patterns and activity patterns of voltage-dependent Ca(2+)-channels were found, suggesting a mechanism for transducing bioelectric signals into cellular responses.Our data suggest that spatial patterning of Vmem, pHi and specific membrane-channel proteins results in bioelectric signals that are supposed to play important roles during oogenesis, e. g. by influencing spatial coordinates, regulating migration processes or modifying the cytoskeletal organization.

View Article: PubMed Central - PubMed

Affiliation: RWTH Aachen University, Institut für Biologie II, Abt. Zoologie und Humanbiologie, Worringerweg 3, 52056, Aachen, Germany. Julia-Krueger@gmx.net.

ABSTRACT

Background: Bioelectric phenomena have been found to exert influence on various developmental and regenerative processes. Little is known about their possible functions and the cellular mechanisms by which they might act during Drosophila oogenesis. In developing follicles, characteristic extracellular current patterns and membrane-potential changes in oocyte and nurse cells have been observed that partly depend on the exchange of protons, potassium ions and sodium ions. These bioelectric properties have been supposed to be related to various processes during oogenesis, e. g. pH-regulation, osmoregulation, cell communication, cell migration, cell proliferation, cell death, vitellogenesis and follicle growth. Analysing in detail the spatial distribution and activity of the relevant ion-transport mechanisms is expected to elucidate the roles that bioelectric phenomena play during oogenesis.

Results: To obtain an overview of bioelectric patterning along the longitudinal and transversal axes of the developing follicle, the spatial distributions of membrane potentials (Vmem), intracellular pH (pHi) and various membrane-channel proteins were studied systematically using fluorescent indicators, fluorescent inhibitors and antisera. During mid-vitellogenic stages 9 to 10B, characteristic, stage-specific Vmem-patterns in the follicle-cell epithelium as well as anteroposterior pHi-gradients in follicle cells and nurse cells were observed. Corresponding distribution patterns of proton pumps (V-ATPases), voltage-dependent L-type Ca(2+)-channels, amiloride-sensitive Na(+)-channels and Na(+),H(+)-exchangers (NHE) and gap-junction proteins (innexin 3) were detected. In particular, six morphologically distinguishable follicle-cell types are characterized on the bioelectric level by differences concerning Vmem and pHi as well as specific compositions of ion channels and carriers. Striking similarities between Vmem-patterns and activity patterns of voltage-dependent Ca(2+)-channels were found, suggesting a mechanism for transducing bioelectric signals into cellular responses. Moreover, gradients of electrical potential and pH were observed within single cells.

Conclusions: Our data suggest that spatial patterning of Vmem, pHi and specific membrane-channel proteins results in bioelectric signals that are supposed to play important roles during oogenesis, e. g. by influencing spatial coordinates, regulating migration processes or modifying the cytoskeletal organization. Characteristic stage-specific changes of bioelectric activity in specialized cell types are correlated with various developmental processes.

No MeSH data available.