Electrically mediated protein movement inDrosophila follicles

Woodruff, Richard I.; Kulp, James H.; LaGaccia, Eric D.

doi:10.1007/bf02439430

Cited by 28 publications

(12 citation statements)

References 24 publications

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“…Roles for electrophoretic movement of morphogens (Cooper, 1984;Cooper et al, 1989;Fear and Stuchly, 1998a-c) have been proposed previously, in the context of follicle-egg systems (Woodruff and Telfer, 1980;Telfer et al, 1981;Bohrmann and Gutzeit, 1987;Woodruff et al, 1988;Woodruff and Cole, 1997;Adler and Woodruff, 2000), self-electrophoresis in Fucus symmetry-breaking (Jaffe et al, 1974;Jaffe and Nuccitelli, 1977), and regeneration in both vertebrate and invertebrate systems (Rose, 1966(Rose, , 1970Smith, 1967;Lange and Steele, 1978). The data on LR patterning suggest a mechanism consistent with this class of models, as applied to a GJC-coupled cell field.…”

Section: Could It Really Work? a Quantitative Model For Electrophoretsupporting

confidence: 64%

Mathematical model of morphogen electrophoresis through gap junctions

Esser

Smith

Weaver

et al. 2006

Developmental Dynamics

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Gap junctional communication is important for embryonic morphogenesis. However, the factors regulating the spatial properties of small molecule signal flows through gap junctions remain poorly understood. Recent data on gap junctions, ion transporters, and serotonin during left-right patterning suggest a specific model: the net unidirectional transfer of small molecules through long-range gap junctional paths driven by an electrophoretic mechanism. However, this concept has only been discussed qualitatively, and it is not known whether such a mechanism can actually establish a gradient within physiological constraints. We review the existing functional data and develop a mathematical model of the flow of serotonin through the early Xenopus embryo under an electrophoretic force generated by ion pumps. Through computer simulation of this process using realistic parameters, we explored quantitatively the dynamics of morphogen movement through gap junctions, confirming the plausibility of the proposed electrophoretic mechanism, which generates a considerable gradient in the available time frame. The model made several testable predictions and revealed properties of robustness, cellular gradients of serotonin, and the dependence of the gradient on several developmental constants. This work quantitatively supports the plausibility of electrophoretic control of morphogen movement through gap junctions during early left-right patterning. This conceptual framework for modeling gap junctional signaling-an epigenetic patterning mechanism of wide relevance in biological regulation-suggests numerous experimental approaches in other patterning systems.

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Section: Could It Really Work? a Quantitative Model For Electrophoretsupporting

confidence: 64%

Mathematical model of morphogen electrophoresis through gap junctions

Esser

Smith

Weaver

et al. 2006

Developmental Dynamics

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“…They found that the potential difference between the oocyte and nurse cells averaged 2.3 mV, with the oocytes being positive with respect to the nurse cells, and again the voltage drop was focused within the intracellular bridges. (35) This difference was highly reproducible and statistically significant at the 0.1% level. They also found that Fly and McFly had the same restricted diffusion as in H. cecropia, based on their respective charge, when microinjected into nurse cells and oocytes of Drosophila follicles.…”

Section: Transport Of Charged Molecules Into the Insect Oocytementioning

confidence: 85%

Left/right, up/down: The role of endogenous electrical fields as directional signals in development, repair and invasion

2003

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A fundamental aspect of biological systems is their spatial organization. In development, regeneration and repair, directional signals are necessary for the proper placement of the components of the organism. Likewise, pathogens that invade other organisms rely on directional signals to target vulnerable areas. It is widely understood that chemical gradients are important directional signals in living systems. Less well recognized are electrical fields, which can also provide directional information. Small, steady electrical fields can directly guide cell movement and growth and can generate chemical gradients of charged macromolecules against the leveling action of diffusion. At the site of a lesion in an ion-transporting epithelium, for example, a substantial electrical field is instantly generated and may extend over many cell diameters. There are numerous other situations in which relatively long-range electrical fields have been shown to exist naturally. Recently, there has been substantial progress in identifying specific processes that are controlled, to some extent, by these endogenous electrical fields. This review highlights these recent data and discusses possible mechanisms by which the fields might affect biological processes.

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“…Previous reports on Drosophila oocytes and their epithelial cells have been in disagreement concerning whether or not dye coupling was present (Woodruff et al, 1988;Verachtert and De Loof, 1989;Woodruff, 1989;Bohrmann and Haas-Assenbaum, 1993). In part, these disagreements derive from differences in detection levels, an issue made more pertinent in the case of Drosophila by the relatively low average coupling ratio of only 64% in control follicles.…”

Section: Discussionmentioning

confidence: 98%

Varied effects of 1‐octanol on gap junctional communication between ovarian epithelial cells and oocytes of Oncopeltus fasciatus, Hyalophora cecropia, and Drosophila melanogaster

Adler¹,

Woodruff²

2000

Arch. Insect Biochem. Physiol.

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In insect gap junctions, species-specific differences occur in response to the purported gap junction uncoupling agent, 1-octanol. Changes in gap junctional communication between oocytes and their epithelial cells following treatment with 1-octanol were assayed in Oncopeltus fasciatus (the milkweed bug), Hyalophora cecropia (the American silk moth), and Drosophila melanogaster. In all three species, microinjection of untreated control follicles with Lucifer yellow CH revealed extensive dye coupling among epithelial cells and between epithelial cells and their oocytes. Also for all three species, treatment with octanol appeared to completely block dye coupling and increase oocyte input resistance. The effect on electrical coupling varied. In Drosophila, octanol diminished the electrical coupling from 64% (0.64 coupling coefficient) in controls to 53% in treated follicles. In Hyalophora, the coupling ratio remained the same following treatment. In Oncopeltus, octanol actually increased the electrical coupling ratio from 84% in controls to 94% in treated follicles. While 0.5 mM octanol left some Oncopeltus epithelial cells dye coupled to the oocyte, the electrical coupling ratio was increased slightly more by this concentration than by 1 or 5 mM octanol solutions, although the differences were not significant. While input resistance (R(o )) increased in all three following treatment with octanol, there was considerable difference in the magnitude of the response. Average oocyte R(o ) for Oncopeltus increased the least of the three species, rising from 196-240 kOhm. Both Hyalophora, with a nearly fourfold increase from 230-900 kOhm or more, and Drosophila, with a twofold increase from 701 kOhm to over 1.2 MegOhm showed much larger changes. Results shown here indicate that insect gap junctions have more varied responses to this common gap junction antagonist than have been reported for their vertebrate counterparts. Arch.

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Electrically mediated protein movement inDrosophila follicles

Cited by 28 publications

References 24 publications

Mathematical model of morphogen electrophoresis through gap junctions

Mathematical model of morphogen electrophoresis through gap junctions

Left/right, up/down: The role of endogenous electrical fields as directional signals in development, repair and invasion

Varied effects of 1‐octanol on gap junctional communication between ovarian epithelial cells and oocytes of Oncopeltus fasciatus, Hyalophora cecropia, and Drosophila melanogaster

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