Ultrastructural Identification of Glial Cells in the Oral Area of the Comb-Bearer Beroё Cucumis M
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Journal of Evolutionary Biochemistry and Physiology, Vol. 40, No. 6, 2004, pp. 710—720. Translated from Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, Vol. 40, No. 6, 2004, pp. 579—588. Original Russian Text Copyright © 2004 by Aronova, Alekseeva. To the 100-Anniversary of A. K. Voskresenskaya Ultrastructural Identification of Glial Cells in the Oral Area of the Comb-Bearer Beroё cucumis M. Z. Aronova and T. M. Alekseeva Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia Received July 4, 2003 Abstract—In the electron microscopic study of oral epithelium and underlying areas of mesoglea of adult comb-bearers Beroё cucumis (Ctenophora), there were described peculiar light cells with a characteristic localization, ultrastructure, ways of interaction with cells of other types including de- veloping and mature chemoreceptors and neuronal processes. Comparison of the obtained results with the literature data allows identification of the light cells as glial cells, one of the first such cells in representatives of the first multicellular animals. INTRODUCTION also be associated with their participation in utili- zation of degenerated chemoreceptors. In an electron microscopic study of mouth epi- This paper presents results of electron micro- thelium of adult comb-bearers Beroё cucumis scopic study of the light cells. Comparison of data (Ctenophora) we have described consecutive stages on their localization and ultrastructural organiza- of chemoreceptor cell maturation [1]. On enter- tion with known morphological characteristics of ing the epithelium from mesoglea the precursor glial elements of the higher multicellular animals cells are transformed into juvenile and then into can help elucidation of the nature of these myste- mature chemoreceptor elements. This results in rious cells revealed on the oral pole of the comb- replacement of damaged and destroyed cells by bearers Beroё cucumis. new cells. Penetration of precursor cells into epi- thelium was preceded by damage of the basement MATERIALS AND METHODS membrane and the appearance of its defects. Near these sites, peculiar light cells were found, which In 15 adult comb-bearers Beroё cucumis (Cteno- were comparable with glial cells by several features phora) kept in sea water, fragments of oral epithe- [1]. Preliminary data indicated possible interaction lium with underlying mesoglea were dissected out. of these cells with developing chemoreceptors and The material was first prefixed in 2–6% glutaral- their role in transfer of precursor elements and dehyde in cacodylate buffer, pH 7.2, at 10°C for nerve endings from mesoglea into the chemorecep- 1–2 h, then, after a quick washing in the same buff- tor epithelium. At the same time, the presence of er, placed in cold 1% OsO4. Contrasting of the fixed phagocyted cell fragments in the cytoplasm can objects with a mixture of 0.5% uranyl acetate and 0022-0930/04/4006-0710 © 2004 MAIK “Nauka/Interperiodica” ULTRASTRUCTURAL IDENTIFICATION OF GLIAL CELLS 711 1% phosphotungstic acid in 70° ethanol was car- both pre- and postsynaptic areas (Fig. 1e). Of spe- ried out in the course of their dehydration. After cial interest was the presence in these sites of me- that, they were embedded in Epon, cut in an LKB soglea and in adjacent parts of receptor epitheli- 812 Ultratome, and examined in JEM 100B, JEM um of cells with cytoplasm of low electron density; 1200EX, and LEO-910 translucent electron mi- we designated them as light cells [1]. Perikarya of croscopes. Besides, there was used the previously these large, relatively not numerous elements had processed experimental material fixed for electron no constant shape, but more often were elongat- microscopic cytochemical study of Beroё epithe- ed, with large cytoplasmic outgrowths, one of lium. This explains the presence of granules of de- them, as a rule, being narrower and longer. No ar- posit appeared in some of presented electron mi- borization of the branches was revealed. In the croscopic photographs. loose cytoplasm with relatively few organelles there were found occasional mitochondria with light RESULTS AND DISCUSSION matrix and a few tubular cristae, moderately de- veloped structures of Golgi apparatus, microtu- Comb-bearers are among the first known mul- bules, rough endoplasmic membranes, lysosomal ticellular animals inhabiting sea water and moving bodies, and small accumulations of osmiophilic actively there with a mouth forth. Resistance of material. The chromatin-filled, bright, large nu- water masses, which is particularly significant dur- clei had, as a rule, triangular shape and centrally ing the high and low tide, and contact with various placed, electron dense, round nucleolus (Fig. 2a). obstacles can lead to a damage of chemoreceptor Synapses between nerve terminals and light cells, cells that are localized at the edge of mouth and regardless of location of these cells—whether in protected from the surface only by layers of glyco- epithelium or in mesoglea—had organization of the calix and mucus. The damaged cells are destroyed, type of synaptic triads, which are characteristic of removed from epithelium, and replaced by new comb-bearers (Figs. 2b–2d). Rather deep invagi- receptor elements. Previously we have found [1] nations of nerve endings into the body of the cyto- that some special light cells participate in the cycle plasmic outgrowth were revealed, predominantly of chemoreceptor development, including its ini- within the limits of the receptor epithelium tial steps associated with reorganization of precur- (Fig. 2e). There was some similarity of the light sor elements. The structure of these cells will be cells with the mesogleal ones. However, in the lat- considered in the present work. ter, also light and with processes and most likely Chemoreceptor cells in the oral epithelium of capable for locomotion and phagocytosis, the cy- Beroё cucumis are known to be distributed non- toplasm was more electron dense. It contained both uniformly—either singly or in groups of several individual microfilaments and their bundles. cells. In the groups there was observed a thicken- Sometimes mitochondria were concentrated in the ing of epithelial layer, whose lower third contained site of transition of the cytoplasm into a thin elec- basal areas of chemoreceptors, mucus-secreting tron dense, clearly seen process containing mi- cells, and juvenile and basal cells. Also located here crofilaments. Nuclei of mesogleal cells, either was a neuropil-like (Fig. 1a) accumulation of pro- elongated or of irregular shape, had a moderate cesses of nerve and receptor cells [1]. Mesoglea electron density. underlying these areas also was found to contain a Light cells were present in various areas of me- similar structure (Fig. 1b). Besides, some process- soglea, but more often in the sites of penetration es of nerve cells and central processes of receptor of precursor cells into the chemoreceptor epithe- cells, the mesogleal, smooth muscular and precur- lium; it is there that we have described them. Pe- sor cells, and interneurons were seen (Figs. 1c, 1d). culiarities of localization of these cells according The cells whose contents indicate their probable to electron microscopic photographs confirmed neurosecretory activity were remarkable. They the suggestion about their interaction with base- were solidly packed with osmiophilic vesicles and ment membrane [1]. Dissolved sites, defects, ap- dark granules and had synapses with nerve endings peared where the light cells were adjacent to the (Figs. 1d, 1e). Synaptic vesicles were clustered in basement membrane. In several sections, the light JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 40 No. 6 2004 712 ARONOVA, ALEKSEEVA Fig. 1. Cellular composition of basal areas of the chemoreceptor epithelium and underlying mesoglea of the comb- bearer. (a) Accumulation of neuropil-type elements (N ) in epithelium; (b) the same in mesoglea (Me), (c) interneurons (IN ) in Me, (d), (e) cell processes with osmiophilic vesicles (COV ), synapses (S ), PC—precursor cells, LC—light cell, LCP—process of the light cell, BM—basal membrane, Nu—nucleus, Nul—nucleolus, BBB—basal body and a basket of interneuron rootlet, MSC—basal area of mucus-secreting cells, M—mitochondria, CC—basal area of chemoreceptor cell. Magnification: (a), (b), (c) 20 000, (d) 23 000, (e) 40 000. JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 40 No. 6 2004 ULTRASTRUCTURAL IDENTIFICATION OF GLIAL CELLS 713 Fig. 1. (Contd.). cells or their processes as well as precursor cells their ontogenesis they were transformed into ma- were already seen in epithelium. Subsequently, ju- ture chemoreceptors. These, in turn, replaced the venile cells also were found here; in the course of damaged degenerated chemoreceptors on moving JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 40 No. 6 2004 714 ARONOVA, ALEKSEEVA Fig. 2. Ultrastructure of light cells (LC) and synapses (S). NT—Nerve terminals, ST—synaptic triad, L—lysosomal bodies. Other designations as those in Fig. 1. Magnification: (a) 25 000, (b) 20 000, (c) 30 000, (d) 20 000. JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 40 No. 6 2004 ULTRASTRUCTURAL IDENTIFICATION OF GLIAL CELLS 715 Fig. 2. (Contd.). to the surface of receptor epithelium [1]. The light bulb base can be surrounded only by the cytoplasm cells also take up and transport nerve endings to outgrowths of the Schwann or supporting cells in- epithelium (Figs. 3a, 3b). Electron microscopic stead of myelin sheaths [2]. pictures indicated a possibility of interaction of the Earlier, when discussing structure of the nervous light cells with the basal cells localized in epitheli- system of comb-bearers, we noted the presence in um [1], as they could be closely adjacent to the lat- it of cells, interneurons [3]. They were revealed ter (Fig. 3c). With time, integrity of the basement most often in epithelium and related sites of me- membrane was restored. soglea of the comb plate and chemoreceptor epi- As mentioned above, the light cell cytoplasm in thelium and much more seldom in the aboral sense some cases contained inclusions similar with frag- organ.