Electrophoretic Repatterning of Charged Cytoplasmic Molecules within Tissues Coupled by Gap Junctions by Externally Applied Electric Fields

Abstract

Ionic currents and cytoplasmic voltage gradients have been observed in a variety of polarizing cells and developing tissues. In certain cases, it has been determined that these endogenous electric fields can segregate intracellular charged molecules by electrophoresis; in other cases, the endogenous fields are suspected to have such an influence. Separate theoretical suggestions have been made that extracellular electric currents, whether from a biological or a nonbiological source, should be able to electrophorese intracellular molecules after being conducted through cell membranes into the interior of long single cells [L. F. Jaffe and R. Nuccitelli (1977) Annu. Rev. Biophys. Bioeng. 6, 445–476], or extended ensembles of cells coupled electrotonically by gap junctions [M. S. Cooper (1984) J. Theor. Biol. 111, 123–130]. To test whether external electric fields could redistribute intracellular molecules within a tissue coupled by gap junctions, and to quantitatively measure in situ the electrophoretic mobility of a charged intracellular molecule, we injected 6-carboxyfluorescein into the electrotonically coupled lateral giant neurons of the crayfish abdominal nerve cord. When a dc electric field (0.2–3.4 V/cm) was subsequently applied along the length of the cord, the negatively charged fluorescent dye was observed to migrate through both the cytoplasms and the gap junctions of the lateral giant neurons, toward the anode, at a rate directly proportional to the applied electric field strength (electrophoretic mobility = −0.92 ± 0.27 μm/sec per V/cm). These results suggest that electric fields of a sufficient magnitude, whether of an exogenous or an endogenous origin, can repattern the distribution of charged molecules within the cytoplasm of an extended ensemble of coupled cells. In addition, these results suggest that externally applied electric fields might be used in studies of pattern formation to repattern the intercellular distribution of charged molecules that are permeant to gap junctions within electrically coupled tissues.

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