Abstract
BackgroundBioelectric 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.ResultsTo 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 Ca2+-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 Ca2+-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.ConclusionsOur 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.
Highlights
Bioelectric phenomena have been found to exert influence on various developmental and regenerative processes
Drosophila follicles consist of 16 germ-line cells - 15 nurse cells (NC) and one oocyte (Ooc) - that are surrounded by a layer of somatic follicle cells (FC)
Gradients of membrane potentials in follicle cells and oocyte Using the potentiometric probe DiBAC, we revealed stage specific Membrane potential (Vmem)-patterns during S9 to S10B by comparing fluorescence intensities in different follicle regions
Summary
Bioelectric phenomena have been found to exert influence on various developmental and regenerative processes. 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. The same holds true for the somatic cells [11], whereas germ-line and somatic cells are interconnected only via gap junctions [12] Besides these communication paths, a variety of intercellular signaling mechanisms play a role during follicle development, since the formation of a mature egg, surrounded by a functional eggshell and containing information for embryonic axes, requires a wealth of specifications as well as patterning and symmetry-breaking steps [13]
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