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Effects of Various Ions on the Action Potentials and on the Excitation-Luminescence Coupling

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Effects of Various Ions on the Action Potentials and on the Excitation-Luminescence Coupling J. exp. Biol. (1980), 88, 219-238 210, ^ith 15 figures W'rinted in Great Britain EXCITABLE EPITHELIAL CELLS IN THE BIOLUMINESCENT SCALES OF A POLYNOID WORM; EFFECTS OF VARIOUS IONS ON THE ACTION POTENTIALS AND ON THE EXCITATION-LUMINESCENCE COUPLING BY ANDRfi BILBAUT University Claude Bernard, Laboratoire d'Histologie et Biologie Tissulaire, 43, Boulevard du 11 Novembre 1918 69622 Villeurbanne Cedex, France {Received 4 February 1980) SUMMARY The bioluminescent scales of the polynoid worm Acholoe astericola are covered with photogenic and non-photogenic excitable epithelial cells which are electrically coupled. The luminescent activity is intracellular and occurs in brief flashes. All the epithelial cells produce non-overshooting action potentials which have been shown to be Na-dependent. In the photo- genic epithelial cells (photocytes) the increase of the stimulus strength elicits another action potential specifically correlated with a flash. This membrane response begins by a fast overshooting Ca-dependent spike potential followed by a Na-dependent secondary depolarization. The excitation- luminescence coupling is dependent on Ca entry into the photocytes. INTRODUCTION Bioluminescence in different animal species can be the result of intracellular activities which are rapidly modulated (Henry & Michelson, 1978). However, very little information is available on the electrophysiological properties of light emitting cells. In Cnidaria, extracellular recordings showed that flashes were correlated with potential changes generated in epithelial or nervous conduction systems (Morin & Cooke, 1971; Anderson & Case, 1975; Bassot et al. 1978). Until recently, the demon- stration of intracellularly recorded membrane activities in light emitting cells has only been obtained in the protozoan Noctiluca (Eckert, 1966) and in larval firefly (Oertel & Case, 1976). In bioluminescent polynoid worms, the luminous activity is intracellular and originates from a single layer of epithelial cells modified as photocytes. These cells have been found suitable for electrophysiological investigations with microelectrodes (Herrera, 1977, 1979; Bilbaut, 1978 a, 1980). The photocytes constitute an homo- geneous cell population, the photogenic area, localized in thin epithelial plates, the scales (elytre), which are inserted dorsally on the worm. These are excitable epithelial •Is (Herrera, 1979; Bilbaut, 1980) which are electrically coupled by numerous gap 22O A. BlLBAUT junctions (Pavans de Ceccatty et al. 1972; Bilbaut, 1980). In the photogenic area* a few photocytes would receive direct excitatory innervation (Herrera, 1979). The photocytes are epithelial effector cells in which the luminescence is triggered by specific excitation of the cell membrane (Herrera, 1979; Bilbaut, 1980). Mem- brane electrogenesis in invertebrate effector cells often appears to require Ca ions. This has been demonstrated in the muscle fibres of crustaceans (Atwood, 1975, for review), annelids (Ito & Tashiro, 1970; Ito, Kuriyama & Tashiro, 1970) and insect larvae (Deitmer & Rathmayer, 1976; Fukuda, Furuyama & Kawa, 1977). An inward Ca current was also observed during the action potential produced in excitable glandular epithelial cells in a Cnidaria (Mackie, 1976). Furthermore, in the effector cells, the activation of effector mechanisms generally involves Ca ions which, in muscle fibres for example, are made available by the calcium influx of the action potential or can be released from intracellular store sites (Ebashi & Endo, 1968). In the photocytes of the polynoid worm Acholoe, two kinds of propagated action potentials can be successively generated after intra- or extracellular stimulation of the preparation (Fig. za and 26). The firing threshold, the amplitude and the wave form of both responses have been shown to be different. One of these action potentials is specifically correlated with the light production (Bilbaut, 1980) which corresponds to a brief flash (Bilbaut & Bassot, 1977). The present study intends to detail the ionic dependence of both action potentials produced in the photocytes in the polynoid worm Acholoe astericola (delle Ch.) and also to characterize the mechanism of the excitation-luminescence coupling. These results have been previously exposed in a short note (Bilbaut, 19786). They indicate principally that (i) an inward Ca current occurs during the action potential correlated with the luminescence, (ii) the light production is dependent on the Ca entry into the photocytes. These data will be compared with the results obtained by Herrera (1979) in the bioluminescent scales of the polynoid worm Hesperonoe. In addition, in the scales of the polynoid worms, the luminous epithelium is in continuity with an excitable and conducting non-photogenic epithelium (Herrera, 1979; Bilbaut, 1980). These common epithelial cells produce action potentials (Fig. zc). In Acholoe, their ionic dependence will also be examined in the present study. MATERIALS AND METHODS Acholoe astericola is a commensal of the starfish Astropecten aurantiacus. The star- fishes were collected by scuba-diving near the Marine Station of Banyuls-sur-Mer and kept in filtered natural sea water at a constant temperature (15 °C). For the experiments, the worms were carefully removed from the starfish and immobilized by cooling. Scales were detached from the worms using fine scissors. The scale diameter is around 1*5-2 mm. The photogenic area lies in a part of the lower plane of the scales. It is surrounded by non-photogenic epithelial cells which also constitute the upper plane of the scales (Fig. 1). Because of the presence of an external collagenous cuticle which prevents the microelectrode penetration into the underlying epithelial cells, the scales were cut in narrow strips (0-5 mm wide A fragment was transported into a dish in which it was maintained in a Bioluminescent scales of a polynoid worm 221 pm n Fig. i. Schematic drawing of the experimental set up. In the middle of the schema, the scale fragment is represented. The photogenic area (black band) lies in part of the lower plane of the scale and in this figure, its limits are delineated by dashed lines. The striped band corresponds to the non-photogenic epithelium. The scale fragment is maintained in a vertical position with two suction electrodes (SE) applied one on each side of the two epithelial faces. The suction electrodes were used as extracellular stimulating electrodes. Other abbreviations: Ir, lumines- cent recording; m, microelectrode; pm, photomultiplier tube; pr, potential recording; r, refer- ence electrode. position by two suction electrodes disposed one on each face (Fig. i). Under these conditions, both epithelial layers were directly accessible to the microelectrodes. The preparations were stimulated extracellularly with either suction electrode. These were made from drawn polyethylene tubing filled with physiological saline solution in contact with silver chloride wire connected to a stimulus isolation unit. Square pulses were delivered to generate the action potentials in the epithelial cells. Intracellular stimulation was not used for the following reasons. In the epithelial cells intracellularly stimulated with double barrelled microelectrodes, the firing threshold for the spike generation was between —20 and +10 mV partly masking the membrane responses (Bilbaut, 1980). When a second microelectrode was placed in another epithelial cell, propagated action potentials were recorded (Herrera, 1979; Bilbaut, 1980). However, attempts showed that it was difficult to hold the micro- electrodes in two epithelial cells for more than 10 or 15 min. These different incon- veniences led to the use of extracellular stimulation only. The recording glass microelectrodes were pulled on a solenoid microelectrode puller (Narishige, PD5) and were filled with 3 M-KC1. Their initial resistance was 40-60 Mfl. They were inserted in an hydraulic microdrive micromanipulator (Narishige, MO 10) and connected to the input of a high-impedance preamplifier. Signals were displayed on an oscilloscope (Tektronix, 5103 N) and an oscillographic chart recorder (Hewlett Packard, 7402 A). The normal saline had the following composition: NaCl, 500 mM; KC1, iomM; CaCl2, 20 mM; MgCl2, 12 mM and Tris (tris-(hydroxyrnethyl)-aminomethane)-HCl fcffer (pH: 7-4), 10 mM. Na-free solutions were achieved by equimolar replacement EXD 88 222 A. BlLBAUT of NaCl by Tris-, choline-, or lithium-chloride. Ca-free solution was obtained b| replacing CaCl2 with NaCl. In solutions where the Ca concentration was lowered, 2 and 10 mM-CaCl2 were added to Ca-free solution and osmotically balanced with NaCl. The Mn saline was obtained by replacing 15 mM-NaCl in the normal solution by an equimolar amount of MnCl2. In Sr or Ba solutions, CaCl2 was substituted by 6 equimolar amounts of SrCl2 or BaCl2. When used, tetrodotoxin (io~ g/ml) or tetraethylammonium chloride (10 mM) was added to the normal saline. Luminescence was collected by an optic fibre light guide positioned over the preparation and connected to a photomultiplier tube (R.C.A. 1 P21). Anode current was displayed on the oscilloscope and chart recorder. In standard conditions, the successive stimulation of the bioluminescence in the scales progressively exhausted the luminous load of the photogenic area. No recovery of the bioluminescent capacities occurring in the isolated scales (Bilbaut & Bassot, 1977), the flash intensity decreased in proportion to the number of electrical pulses applied to the preparations. During
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