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Cell Junctions in the Excitable Epithelium of Bioluminescent Scales on a Polynoid Worm: a Freeze-Fracture and Electrophysiological Study

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Cell Junctions in the Excitable Epithelium of Bioluminescent Scales on a Polynoid Worm: a Freeze-Fracture and Electrophysiological Study J. Cell Sci. 41, 341-368 (1980) 341 Printed in Great Britain © Company of Biologists Limited 1980 CELL JUNCTIONS IN THE EXCITABLE EPITHELIUM OF BIOLUMINESCENT SCALES ON A POLYNOID WORM: A FREEZE-FRACTURE AND ELECTROPHYSIOLOGICAL STUDY A. BILBAUT Laboratoire d'Histologie et Biologie Tissulaire, University Claude Bernard, 43 Bd. du 11 Novembre 1918 69621, ViUeurbairne, France. SUMMARY The bioluminescent scales of the polynoid worm Acholoe are covered by a dorsal and ventral monolayer of epithelium. The luminous activity is intracellular and arises from the ventral epithelial cells, which are modified as photocytes. Photogenic and non-photogenic epithelial cells have been examined with regard to intercellular junctions and electrophysiological properties. Desmosomes, septate and gap junctions are described between all the epithelial cells. Lan- thanum impregnation and freeze-fracture reveal that the septate junctions belong to the pleated- type found in molluscs, arthropods and other annelid tissues. Freeze-fractured gap junctions show polygonal arrays of membrane particles on the P face and complementary pits on the E face. Gap junctions are of the P type as reported in vertebrate, mollusc and some annelid tissues, d.c. pulses injected intracellularly into an epithelial cell are recorded in neighbouring cells. Intracellular current passage also induces propagated non-overshooting action potentials in all the epithelial cells; in photocytes, an increase of injected current elicits another response which is a propagated 2-component overshooting action potential correlated with luminous activity. This study shows the coexistence of septate and gap junctions in a conducting and excitable invertebrate epithelium. The results are discussed in relation to the functional roles of inter- cellular junctions in invertebrate epithelia. It is concluded that the gap junctions found in this excitable epithelium represent the structural sites of the cell-to-cell propagation of action potentials. INTRODUCTION Three classical types of intercellular junctions are generally described in inverte- brate epithelia. These are desmosomes, septate and gap junctions (Staehelin, 1974). Desmosomes and gap junctions can be demonstrated in a large variety of invertebrate and vertebrate tissues (Staehelin, 1974; Larsen, 1977) while septate junctions have rarely been reported in vertebrate tissues (Connell, 1978). Electrophysiological investigations, using intracellular recording and tracer injection, demonstrated ionic and metabolic coupling between non-excitable adjacent cells in invertebrate (Loewen- stein & Kano, 1964; Loewenstein, 1976) and vertebrate (Petersen, 1976; Hammer & Sheridan, 1978) glandular epithelia. The cell-to-cell propagation of action potentials has been described in invertebrate and vertebrate excitable tissues such as epithelia (Mackie, 1965, 1976; Roberts & Stirling, 1971; Kater, Rued & Murphy, 1978), cardiac and smooth muscle (Barr, Dewey & Berger, 1965; Barr, Berger & Dewey, 342 A. Bilbaut 1968) and nervous electrical synapses (Watanabe & Grundfest, 1961; Bennett, Naka- jima & Pappas, 1967). Cell coupling in both non-excitable and excitable tissues involves low-resistance pathways which have been correlated, in many instances, with the presence of gap junctions (Bennett, 1978). In invertebrate epithelia there is no direct evidence that the gap junctions act as coupling sites or are the only coupling sites (Satir & Gilula, 1973; Staehelin, 1974; Bennett, 1978); this will be discussed in a later section. The object of the present study is to characterize intercellular junctional structures found in an invertebrate epithelium which has conducting, excitable and biolumine- scent properties. The polynoid worm Acholoe astericola (dell Ch) displays strong luminous activities after electrical or mechanical stimulation. Spontaneous light emission has never been observed in Acholoe and the significance of the biolumine- scence in all the polynoid worms studied remains purely speculative (Haswell, 1882; Nicol, 1953). In Acholoe, luminous activities originate in the scales (elytra) which are thin, epithelial diskoidal plates arranged dorsally in a double row. Each is attached to a segment by a short peduncle and consists of a simple-layered continuous epithelium covered by a collagenous cuticle. On the ventral face, the epithelial cells are differen- tiated as photocytes which constitute a homogeneous cell population, the photogenic area. Photocytes contain several granules of paracrystalline endoplasmic reticulum (Bassot, 1966) which are the intracellular sources of the bioluminescent activity of the scales (Bassot & Bilbaut, 1977a). Pavans de Ceccatty, Bassot, Bilbaut & Nicolas (1977) reported that the 2 epithelial planes delimit an internal compartment crossed by multiple cellular processes arranged perpendicularly on both epithelial faces. These processes originate from the basal pole of all the epithelial cells and also from a special cell type found in the internal compartment, the 'clear cells'. All the processes contain bundles of filaments. Nerve trunks arise from a ganglion near to the centre of the scale and end at numerous peripheral sensory cells. An extracellular electrical pulse applied to the photogenic area of an isolated scale produces at least one brief flash (60-120 ms in duration). During repetitive electrical stimulation (1 pulse/s), the intensity of successive flashes at first increases rapidly, for a short period, then decreases slowly (Bilbaut & Bassot, 1977). Autophotographic observations after image intensification of the photogenic area show several striking features (Bassot & Bilbaut, 19776). Firstly, during one flash, the illumination starts at the stimulated site and spreads towards the periphery of the luminous effector. Secondly, at the beginning of a repetitively stimulated light emission, only a part of the photogenic area is illuminated. This active zone is initially limited to an area close to the stimulated site and, flash by flash, increases gradually in extent. When the flash intensities reach their maximum value, the whole of the photogenic area is illumin- ated. The slow decline of the luminous intensities of flashes results from the progressive exhaustion of bioluminescent products. No recovery of bioluminescent capacities occurs in isolated scales (Bilbaut & Bassot, 1977). Luminescent propagation in the photogenic area could result from the presence of either a multi-innervated uncoupled epithelial cell system or a conducting epithelial cell system. Ultrastructural observations (Pavans de Ceccatty et al. 1977) did not Cell junctions in excitable epithelium 343 demonstrate terminal neuro-effector junctions ending on photocytes, whereas numerous cell junctions, both septate and gap junctions, were found between all epithelial cells, supporting the possibility of a conducting epithelial system. Cell coupling and cell excitability have been reported in photogenic and non- photogenic epithelial cells in Acholoe (Bilbaut, 1978 a) in a preliminary account and Herrera (1977, 1979) has also reported action potential propagation in the biolumines- cent scale epithelium of the polynoid worm Hesperonoe. In the present paper, the morphology of all the cell junctions found in the scale epithelium is detailed in the first section, using intercellular tracer and freeze-fracture techniques. In the second section, electrical coupling and excitability of epithelial cells are examined using intracellular recording and stimulation techniques. MATERIALS AND METHODS Acholoe astericola is a commensal of the starfish Astropecten aurantiacus. The starfishes were collected by scuba-diving near the Marine Station of Banyuls-sur-Mer and transported in isothermic boxes to Lyon. They were maintained in natural seawater at a constant temperature (15 °C) and fed monthly with clams. In order to avoid damage to the annelid during the sampling of the scales, worms were carefully removed from the starfish, transferred to a Petri dish filled with seawater and placed in a freezer. When the first ice-crystals appeared in the seawater, worms were immobilized for a few minutes and individual scales were cut off using fine scissors. Scanning electron microscopy Scales were fixed by immersion for 60 min at room temperature in 3 % glutaraldehyde in o-i M Na cacodylate-HCl buffer, pH 7-4, containing 0-3 M NaCl. The cuticle covering the scale was carefully peeled off on one of the epithelial faces in the washing solution (0-3 M NaCl in 02 M Na cacodylate-HCl buffer at pH 7'4). Cuticle pieces with adhering epithelium were dehydrated in acetone and critical-point dried (acetone-CO| substitution). Observations of preparations were made with a Cambridge (S600) scanning electron microscope. Transmission electron microscopy For conventional fixation, the scales were cut into small pieces, fixed and washed for 1 h according to the above procedure, postfixed for 1 h at room temperature in 1 % osmium tetroxide and 0-4 M NaCl buffered by o-i M Na cacodylate-HCl at pH 7-4, dehydrated and embedded in epoxy resin. Thin sections were stained with uranyl acetate and lead citrate before examination. The lanthanum solution was prepared using Revel & Karnovsky's method (1967); fixed and rinsed specimens were postfixed for 4 h at room temperature. After dehydration and embedding, thin sections were lightly stained with lead citrate. Freeze-fracturing Whole scales were fixed for 1 h in glutaraldehyde solution, washed for 30 min in NaCl buffered solution then immersed
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