The ciliated sensory cell of Stauridiosarsia producta (Cnidaria, Hydrozoa} - a nematocyst-free nematocyte?
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1 Zoomorphology (1994) 114: Springer-Verlag 1994 Rainer Golz - Ulrich Thurm The ciliated sensory cell of Stauridiosarsia producta (Cnidaria, Hydrozoa} - a nematocyst-free nematocyte? Accepted 9 April i994 Summary A mechanosensitive ciliated cell type of the polyp Stauridiosarsia producta (Hydrozoa) was investigated by means of electron microscopy. These cells bear at their apical cell surface a modified cilium, a set of seven stereovilli, a so-called pseudovillar system and a large vacuole. Cilium and stereovilli are interconnected like the cnidocil apparatus of hydrozoan nematocytes which is responsible for mechanoelectric transduction. The vacuole is enclosed by and linked to the pseudovillar system by a microtubular basket. Considering its structural organization and physiological activities the ciliated sensory cell closely resembles a nematocyte that has lost its ability to produce a nematocyst. A. Introduction Cnidarian organisms usually contain different types of ciliated cells within their epithelia. Frequently, the epitheliomuscular ceils themselves bear motile cilia on their apical surface (see, for example, Golz and Thurm 1993). A few other cell types, however, are described bearing structurally modified, immotile cilia (Westfall 1973; Golz and Thurm 1991a, 1993). Most prominent within this group are the nematocytes. Their cilia, especially those of hydrozoan nematocytes, were shown to be extremely modified, containing up to 200 microtubules and an additional cross-striated central filament body (Slautterback 1967; Cormier and Hessinger 1980). Since the explosive discharge of their nematocyst (Holstein and Tardent 1984) is usually triggered by mechanical forces applied to the cnidocil apparatus, the nematocytes were supposed to be mechanosensitive cells (Holstein and Hausmann 1988). This assumption was only recently confirmed by direct electrophysiological measurements on nematocytes of the marine hydro- R. Golz (1~]) 9 U. Thurm Institut f/jr Neuro- und Verhaltensbiologie, Westffilische Wilhelms-Universit/it, Badestrasse 9, D Mtinster, Germany zoon Stauridiosarsia producta. In response to mechanical stimulation of their cnidocil apparatus, these cells produce receptor potentials like other mechanosensitive cells such as vertebrate hair cells or insect mechanoreceptors (Brinkmann and Thurm 1993; Brinkmann et al. 1994). As shown by previous electron microscopic investigations, the hydrozoan cnidocil apparatus consists of a set of stereovilli (= large microvilli) surrounding a central modified cilium, the cnidocil (Slautterback 1967; Hausmann and Holstein 1985). Within a short contact region of up to 1 gm in height, both structures are linked by intermembrane connectors. In the same region, stereovillar and cnidociliary membranes are tightly connected to their underlying axonemes by periodically arranged cross-bridges (Golz and Thurm 1991b). As far as investigated, this constructional scheme seems to be common to almost all ciliated mechanoreceptor cells in cnidarians and in other invertebrates (Budelmann 1989; Golz and Thurm 1991a, 1993). Considering ultrastructural and electrophysiological data, mechanical stimuli acting on the cilium-stereovillus complex are thought to cause stress between the cilium and its stereovillar support that is concentrated via the intermembrane connectors on membrane-integrated transducing ion channels (Golz and Thurm 1991b; Brinkmann et al. 1994). Our ultrastructural investigations of S. producta revealed that these polyps contain another cell type with a modified cilium in addition to their nematocytes. This cell type corresponds to a ciliated mechanosensory cell of Coryne pintneri Schneider, 1897, a close relative of S. producta (see Tardent and Schmid 1972). While our data concerning the gross morphology and the cellular environment of the sensory cell coincide with those obtained by Tardent and Schmid, we obtained different information about the architecture of the apical cell pole which will be presented in this paper. We will provide evidence that this type of cell is more closely related to nematocytes than to other types of mechanosensory cells.
2 186 Fig. 1 Live ciliated sensory cell in a filiform tentacle of Stauridiosarsia produeta. Nomarski interference contrast. The tip of the cilium is marked by an arrow, the stereovillar cone by an open arrow. The apical vacuole is indicated by an arrowhead Figs. 2-5 Electron micrographs of ciliated sensory cells Fig. 2 Cell with elongated shape in the head of a capitate tentacle. Its apical surface bears the cilium-stereovillus complex (CS). The cytoplasm is traversed by ER-like tubes (arrows). Nu nucleus, V vacuole Fig. 3 Cell in the stalk of a capitate tentacle. The cell has a pyramidal shape. Its basal membrane (arrowheads) is in contact with neurites (N). The mesoglea is marked by arrows. Nu nucleus, V vacuole Fig. 4 Sensory cell (SC) innervated by an efferent synapse. The dense-cored synaptic vesicles are bordered by open arrows. Note the large, membrane-containing vesicles in the basal portion of the sensory cell Fig. 5 Part of the basolateral cytoplasm. It contains numerous tubes of the endoplasmic reticulum (ER). Nu nucleus
3 187 B. Materials and methods Stauridiosarsia producta (Wright 1858) was cultivated in artificial sea-water at about 14 ~ C. The polyps were fed once a week with freshly hatched Artemia salina. All specimens are descendents of a single colony obtained from the Biological Station of Helgoland. For electron microscopy, polyps were cut offfrom their stolons and transferred into artificial, calcium-free sea-water supplemented up to 90 mm with MgC12 to prevent fixation-induced contractions. The polyps were fixed with 5% glutaraldehyde, 2% formaldehyde, 10% DMSO, 5 mm EGTA, and 0.5% tannic acid in 0.1 M sodium cacodylate buffer (ph 7.4) for 30 min. The specimens were rinsed with the same buffer and subsequently washed with sodium cacodylate buffer at ph 6.0. After postfixation for 15 rain with 5% tannic acid and 0.5% glutaraldehyde in this buffer, they were rinsed and stained with 1% OsO4 and 0.025% ruthenium red in 50 mm sodium cacodylate buffer (ph 6.0) for 5 rain. During dehydration in a graded series of ethanol, the polyps were stained for 15 min by exposure to 1% uranyl acetate in 70% Figs. 6, 7 Serial longitudinal sections of a migrating sensory cell. The cell is extremely elongated. Its cilium (C) and stereovilli (S) are reduced in length and completely separated by the extracellular matrix (e). Vacuole (1O and nucleus (Nu) are separated by a broad cytoplasmic zone containing mitochondria (Mi). P pseudovillus, M microtubules, B basal body Fig. 8 Migrating cell in a later developmental stage. The cell body has attained its final shape. The cell migrates along the mesoglea (marked by arrows). En endoderm Fig. 9 Apical part of a tissue-integrated cell. The cilium (C) has reached its full length. The stereovilli (S) are now longer than the cylinder formed by the extracellular matrix (e). A central filament body (F) stabilizes the cilium. B basal body, Vvacuole
4 188 ethanol. The specimens were embedded in Spurr's resin following standard procedures. Ultrathin sections were made with a diamond knife on a MT 7000 microtome (Microm), poststained with lead citrate, and examined in a Philips EM 201 equipped with a goniometer stage. C. Results I. Gross morphology The ciliated mechanosensory cell of S. producta (Fig. 1) is characterized by an apical cilium-stereovilli (CS) complex and a large, electron-lucent vacuole located between the nucleus and the CS complex. The cells bear an extremely long cilium of up to 50 pm which, however, adapts in length to changes in environmental conditions. The ciliated sensory cells are integrated into the ectodermal cell layer of the filiform (-- sensory) tentacles and of the stalks and heads of the capitate tentacles (for a detailed description of the morphology of this polyp see Stoessel and Tardent 1971, Golz 1994). Since the sensory tentacles and the stalks of the capitate tentacles are formed by more flattened epitheliomuscular cells than the head of the capitate tentacles, the corresponding ciliated sensory cells are slightly different in shape. Their pyramidal form in the filiform tentacles and in the stalks of the capitate tentacles (Fig. 3) is replaced by more elongated shapes in the heads of the tentacles (Fig. 2). At their bases, the ciliated sensory cells are in intimate contact with neurites (Figs. 3, 4). While so far no afferent synaptic connections have been found, the sensory cells themselves appear to be innervated by efferent synapses (Fig. 4). At the site of efferent innervation, the cells contain some large vesicles (Figs. 2 4) which may contain some additional membranous material (Fig. 4). In its basolateral portions, the cytoplasm contains numerous tube-like cisterns of the endoplasmic reticulum (Figs. 2, 5), whereas the apical portion of the cell is dominated by the single, large vacuole (Figs. 3, 9, 15). This electron-lucent vacuole has a diameter of approximately 1.8 pm. It is bordered by a vacuolar membrane and is filled with slightly contrasted fuzzy material (Figs. 8, 10, 16). In most instances, the vacuole is closely apposed to the nucleus. Its membrane and the nuclear envelope are separated by a thin cytoplasmic layer only. Like nematocytes, the ciliated sensory cells actively migrate through the ectodermal cell layer at or in the vicinity of the mesoglea (Figs. 6, 8). Migrating cells found in more basal parts of the hydranths have obviously become fixed in earlier states of their development, since their vacuole and nucleus are still separated by a broad zone of organelle-filled cytoplasm (Fig. 6). The extremely elongated shape of these cells is maintained by a cylinder of longitudinally arranged microtubules surrounding nucleus, mitochondria, and vacuole. With their distal parts, these microtubules are tightly interconnected to the apical CS complex (Figs. 6, 7). On th e way to their site of destination, the migrating cells receive their final form: nucleus, vacuole, and apical cytoskeletal apparatus are then aligned like those of tissue-integrated cells. In the latter state, the cylindrical arrangement of microtubules is still present. In contrast to tissue-integrated cells, the migrating cells contain only short ciliary stubs which surmound the surrounding stereovilli by less than one micrometer (cf. Figs. 6, 9). These cilia, however, start to grow out to full length as soon as the cells become integrated into the ectodermal cell layer. The apical surface of the ciliated sensory cell is formed by two closely interconnected cytoskeletal systems: the CS complex and the pseudovillar system. To facilitate the understanding of the complicated structural organization of the apical cell surface, all data obtained from cross- and longitudinal sections are summarized and presented in a schematic reconstruction (Fig. 22). II. CS complex The slender and modified cilium originates from the top of a flat cone-like protrusion at the apical cell surface (Figs. 9, 12). This protrusion is maintained by electrondense cytoskeletal elements of the pseudovillar system (see below). The ciliary origin, i.e., its basal body, and the cone-like apical cell surface are separated by a constriction of the ciliary shaft giving the impression that the basal body is located within the cilium itself. The ciliary axoneme consists of nine or a few more dynein-free microtubule doublets and up to 15 additional singular microtubules (Figs ). The longitudinal axis of the cilium is marked by a cross-striated electrondense rod (Figs. 9, 14). This structure has a similar stria- Figs Longitudinal sections through the apical cell pole Fig. 10 Part of Fig. 3 in higher magnification. The cilium (C) is encircled by pseudovilli (P) and stereovilli (S). The extracellular matrix (e) is anchored at the pseudovillar membrane. The stereovillar cores terminate (arrow) beside the vacuole (l/}. Small vesicles fuse with the vacuole (open arrow). E epitheliomuscular cell Fig. 11 The pseudovilli (P) have a periodically striated central core. They are in intimate contact with the stereovilli (S). Electrondense lamellae (arrows) are situated between and connected to the pseudovilli, e extracellular matrix Fig. 12 Pseudovillar system. The pseudovilli (P) terminate (open arrow) at the microtubular basket (MB). Electron-dense lamellae (L) are oriented toward the center of the system. A disk (D) within a ciliary constriction separates basal body (B) and a cone-like protrusion of the apical surface. The basal plate of the cilium is marked by an arrow. The apical part of the vacuolar membrane becomes aligned to the microtubular basket (small arrows), e extracellular matrix Fig. 13 The vacuolar membrane is linked to a microtubule (arrowhead) of the basket by cross-bridges (arrows). The microtubules are embedded in an electron-dense cement Fig. 14 Contact region between stereovilli (S) and cilium (C). The complete CS complex is surrounded by a collar of the epitheliomuscular cell (E). The cilium is stiffened by a central filament body (F). Above the extracellular matrix (e), cilium and stereovilli become linked by fibrous connectors (arrows)
5 189 tion pattern to the central filament body in the cnidocil of hydrozoan nematocytes. With the exception of the nine microtubule doublets that arise from the triplets of the basal body all additional axonemal components emerge from the ciliary basal plate (Fig. 12). In most instances, the modified cilium is surrounded by seven stereovilli of ca. 2 gm length (Figs. 2, 9, 10, 14). The stereovilli are stabilized by a central rod of densely packed filaments. As known from homologue systems, the central cores consist of highly cross-linked actin filaments. For half of their length, the stereovillar cores are anchored within the apical part of the cell (Figs. 3, 10).
6 190
7 191 sc f I microlubule, iii IIII oo.n cores _~ pseudovillar rods 0~ filament body Fig. 22 Schematic reconstruction of the apical cell portion. B basal body, C cilium, Mt cross-sectioned microtubules, P pseudovillus, S stereovillus, Vvacuole, e extracellular matrix. Besides the longitudinal section, arrowheads indicate the planes of the corresponding cross-sections Figs Serial cross-sections of the apical cell part Fig. 15 The cytoplasm around the basal parts of the vacuole (10 contains numerous small vesicles (arrows). The cellular shape is maintained by a cylindrical arrangement of microtubules (M) Fig. 16 The apical membrane of the vacuole is covered by a microtubular basket (arrowheads). The rods of the pseudovilli (some of them are marked by small arrows) are encircled by the bases of the seven stereovilli (indicated by arrows) Fig. 17 Each stereovillus (arrow) is associated with a pair of pseudovilli (small arrows). They are interconnected by electron-dense bridges (arrowheads). The pseudovilli are associated with electrondense lamellae (L). All lamellae are interconnected by electrondense ropes or bars (open arrows) Fig. 18 Cross-sectioned microtubular basket associated with the vacuolar membrane (open arrow). The microtubules (arrowheads) are embedded in an electron-dense cement. The basal end of a pseudovillus is marked by an arrow Fig. 19 Proximal part of the CS complex. The ciliated sensory cell is enclosed by a single epitheliomuscular cell (E). The stereovilli (S) are separated from the central cilium by the extracellular matrix (e) Fig. 20 Distal part of the contact region. Stereovilli and cilium are linked by fibrous material (arrows). E epitheliomuscular cell Fig. 21 Cilium within the cuticle of the polyp. The cuticle contains brush-like structural units (U). The ciliary axoneme consists of dynein-free microtubule doublets (arrowhead), additional microtubules (arrows), and the central filament body (F) The basal portions of stereovilli and cilium are separated by a short extracellular cylinder composed of a cross-striated material (Figs. 3, 6, 10, 19). Due to its restricted height of only 1.3 gm, this extracellular matrix allows the formation of a short contact region between the tips of the stereovilli and a corresponding portion of the cilium (Figs. 14, 20). Within this contact region, the distal parts of the stereovilli are forced by their glycocalyx into a closed cylindrical arrangement, the stereovillar cone. Stereovillar cone and cilium are held in a concentric position by fibrous components of their membrane coats, the intermembrane connectors (Figs. 14, 20). Even in migrating cells, the extracellular matrix separates cilium and stereovilli. Here, however, both components are still completely separated because of their reduced length (Figs. 6, 7). The cross-striated extracellular matrix is anchored at the apical cell surface by its close association to the pseudovillar membranes (Figs. 9, 10). III. Pseudovillar system The most extraordinary components at the apical surface are small microvillus-like protrusions. Since these protrusions resemble microvilli only in shape but not in the composition of their central cores, they have been called pseudovilli (Golz and Thurm 1993). These protrusions, up to 300 nm long, contain cross-striated central rods that elongate for about 500 nm into the cytoplasm. In electron density and periodical arrangement
8 192 of their subunits, the rods are clearly distinguishable from the stereovillar cores but are similar to the pseudovilli of nematocytes (Fig. 11). In the ciliated sensory cells of S. producta, 14 pseudovilli form a ring-like system between the stereovillar cone and the cilium (Figs. 10, 16). Each stereovillus is linked to a pair of pseudovilli by short electron-dense ribbons. Electron-dense lamellae emerge from the side of the pseudovillar cores (Figs. 16, 17). Like spokes of a wheel they are directed toward the center of the pseudovillar arrangement. Adjacent lamellae are additionally interconnected by a complex system of dectron-dense bars or ropes (see Fig. 22). Some globular extensions of the electron-dense lamellae project into the cone-like basement of the cilium. A small electron-dense disk terminates the cone exactly within the constriction of the ciliary shaft. The proximal ends of the pseudovillar rods terminate at the microtubular basket which covers the apical membrane of the vacuole (Fig. 12). the cellular environment of these cells are identical in both organisms, some differences in their ultrastructural appearance have to be explained. Some of these differences, as for example the number of stereovilli, are obviously species-specific. The CS complexes reveal a nine-fold symmetry in C. pintneri, but are composed of only seven radially arranged segments in S. producta. The assumption of Tardent and Schmid, however, that the cilium has no structural subunits and their description of a bifurcated basis of the stereovilli (without an indication of the occurrence of pseudovilli) are based on electron microscopical investigations of cells that have been fixed with a relatively rough fixation technique. Considering our ultrastructural data, Tardent and Schmid's reconstruction of the apical cell surface of this type of sensory cell has therefore to be modified. In S. producta, and surely also in C. pintneri, the ciliated sensory cell bears a cilium with a microtubule-based axoneme, a set of actin-containing stereovilli, and, additionally, the pseudovillar system. IV. Vacuole The cytoplasm around the vacuole is filled with small vesicles. While some of these are filled with the same material as the ER-like tubes, the content of other vesicles is similar to the electron-lucent content of the central vacuole. These latter vesicles frequently seem to fuse with the basal parts of the vacuolar membrane. The vacuole itself seems to be under internal pressure, since it is able to deform the adjacent nuclear envelope by its basal portion (Fig. i0). Vacuole and pseudovillar system are indirectly linked by microtubules covering the distal half of the vacuolar membrane. This membrane domain is bordered by and linked to a microtubular basket (Figs. 10, 13, 18). The basket has a cone-like shape and consists of microtubules which are embedded in an electron-dense cement (Fig. 18). The microtubular basket and the pseudovillar system are tightly interconnected. The bases of the pseudovilli terminate at or near the microtubules and the spoke-like lamellae are directly attached to the microtubular basket. Because of its tight connection to the microtubular basket, the vacuolar membrane is forced into the same cone-like configuration (Figs. 10, 12). D. Discussion I. Cellular architecture Ultrastructural investigations and in vivo observations on the ciliated sensory cells of the hydrozoan polyps C. pintneri (see Stoessel and Tardent 1971; Tardent and Schmid 1972) and S. producta (see Golz 1994; this paper) indicate that both cells represent the same type of mechanosensitive cell. While the gross morphology and II. Cilium and stereovilli The cilium of the mechanosensory cell of S. producta reveals the same structural modifications as the cnidocils of hydrozoan nematocytes: additional microtubules, the lack of dynein, and the occurrence of the cross-striated central filament body (Golz and Thurm 1991b; Brinkmann etal. 1994). In contrast to the cnidocils and most other cilia, the cilium of the mechanosensory cell of S. producta is linked to the cellular surface in an extraordinary mode: it appears to be mechanically uncoupled from the intracellular cytoskeleton by a constriction beneath its basal body. By this dislocation of the basal body toward the ciliary shaft and by the lack of ciliary rootlets, only weak mechanical resistance may oppose any deflections of the cilium caused by externally applied mechanical stimuli. In S. producta, nematocytes and sensory cells always have the same number of seven stereovilli (Brinkmann et al. 1994). The CS complex of nematocytes, however, has a concentric appearance only on its distal portion, while the proximal portions of the stereovilli are forced into a horseshoe-like configuration by the voluminous nematocyst. In contrast to this arrangement, the vacuole of the sensory cell is concentrically localized to the cilium. III. Structural and functional similarities to nematocytes While the CS complex is a common component of a great number of different types of epithelial mechanoreceptors known as collared cell type (Budelmann 1989), the ciliated sensory cells studied here share some unusual cellular components, the pseudovilli, with only one other type of mechanosensitive cell, the nematocyte. To
9 193 our knowledge, no other cell type has developed a cytoskeletal system similar to the complex pseudovillar system. While cross-striated elements with different functions are frequently associated with the basal bodies of cilia and flagella in unicellular and multicellular organisms, the formation of microvilli-like protrusions and the mode of their interconnection are restricted to pseudovilli. In the sensory cell and also in the nematocyte, the pseudovillar system is not only tightly associated with the same type of extracellular matrix separating the basal portions of stereovilli and cilium (Golz and Thurm 1991b) but is also connected with a complex microtubular basket surrounding a voluminous vacuole (Stidwill and Honegger 1989). While in nematocytes this vacuole is filled with an extra ordinarily large and complex content, the nematocyst (for review see Mariscal 1974), such a content is not formed within the vacuole of the ciliated sensory cells. Similar to nematocysts (Weber 1989), however, its content seems to be under internal pressure as indicated by its shape and influence on adjacent organelles. Nematocytes are mechanosensory cells that are directly involved in prey capture, locomotion, and defense. These functions depend on the discharge of the nematocysts, since only by this process can the venomous content of the capsule become ejected, or the sticky capsular tube come into contact with prey organisms or the substratum (Mariscal 1974; Tardent and Holstein 1982). To prevent a premature loss of discharged nematocysts, this organelle has to be firmly anchored within the cell and its surrounding tissue. This function is achieved by a complex microtubular cytoskeleton (Wood and Novak 1982; Stidwill and Honegger 1989) and, possibly, by the pseudovillar system. This latter cytoskeletal component may additionally be responsible for the correct positioning of the nematocyst at the apical surface of the nematocyte. Since the various types of nematocytes contain a pseudovillar system ( with its closely associated extracellular matrix), these cytoskeletal elements are supposed to be evolved together with the nematocysts to form a functional unit. Plesiomorphic nematocytes might have differentiated from early mechanosensitive cells by the simultaneous development of cyst and pseudovillar system. Even in the morphogenesis of nematocytes of recent hydrozoa, cyst formation and cytoskeletal differentiation are simultaneous processes influencing one and another. Microtubules, especially, are involved in the formation and probably in the invagination of the nematocyst's tube (Holstein 1981). As mentioned above, we frequently found immature cells migrating in the body column of S. producta. Although so far no information is available concerning the very early state of cellular development, we may state that the changes in cellular shape during their integration into the tissue are also mediated by a microtubular system, the cylindrical bundle described in Figs. 6, 7. Synapses of hydrozoan organisms are usually char- acterized by RFamide-containing, dense-cored vesicles that are bound to the synaptic membrane by osmiophilic material (Koizumi et al. 1989). As indicated by immunofluorescence microscopy using antibodies against RFamides, this type of neurotransmitter seems to be expressed in all neurons of S. producta but is not localized in the ciliated sensory cell and the nematocytes (Golz 1994). These data are supported by our electron microscopical investigations of the ciliated sensory cells of S. producta which were shown to be postsynaptically coupled to efferent neurons but did not contain densecored vesicles. The same situation occurs in nematocytes of hydrozoa; while their efferent innervation was directly revealed by ultrastructural methods (Westfall 1988) and has been confirmed by electrophysiological measurements (Brinkmann and Thurm 1993), the formation of presynaptic-like connections is indicated by electrophysiological measurements only (Brinkmann and Thurm 1993). Since so far no ultrastructural correlates have been found, the signal transmission from the nematocyte (and possibly also from the ciliated sensory cell) to the neuronal network is supposed to depend on a synapse-independent mode of exocytosis. Considering the fact that the ciliated sensory cells of S. producta contain a pseudovillar system closely associated with a microtubular basket and a large vacuole and the observation that neuronal interactions similar to those of nematocytes occur, the ciliated sensory cells may represent some conserved evolutionary intermediate state toward a nematocyte that has not yet evolved the ability to form a cyst but is still used as sensory cell, or, more likely, as a step backward. Then, these cells would be "nematocytes" that can still express the genomic information for the sensory apparatus and the associated cytoskeleton but not for the capsular content. Acknowledgements We are indebted to Mrs. Otterbein for technical assistance and to M. Brinkmann for cultivating S. producta. The work was supported by Deutsche Forschungsgemeinschaft (SFB 310) and DFG-grant Go 623/1-1. References Brinkmann M, Thurm U (1993) Mechanoreceptive properties of hydrozoan nematocy~es in situ. In: Elsner N, Heisenberg M (eds) Proc 21st G6ttingen neurobiol conf. Thieme, Stuttgart, p 155 Brinkmann M, Golz R, Thurm U (1994) Determination of the site of mechanoelectrical transduction in the nematocytes of Stauridiosarsia by combined electrophysiological and ultrastructural investigations. Elsner N, Breer H (eds) Proc 22nd G6ttingen neurobiol conf. Thieme, Stuttgart, p 67 Budelmann BU (1989) Hydrodynamic receptor systems in invertebrates. In: Coombs S, G6rner P, Mfinz H (eds) The mechanosensory lateral line. Neurobiology and evolution. Springer, New York, pp Cormier SM, Hessinger DA (1980) Cnidocil apparatus: Sensory receptor of Physalia nematocytes. J Ultrastruct Res 72:13-19
10 194 Golz R (1994) Occurrence and distribution of RFamide-positive neurons within the polyps of Coryne sp. (Hydrozoa, Corynidae). Biol Bull 186: Golz R, Thurm U (1991 a) Cytoskeletal modifications of the sensorimotor-interneurons of Hydra vulgaris (Cnidaria, Hydrozoa), indicating a sensory function similar to chordotonal receptors of insects. Zoomorphology 111: Golz R, Thurm U (1991b) Cytoskeleton-membrane interactions in the cnidocil complex of hydrozoan nematocytes. Cell Tissue Res 263: Golz R, Thurm U (1993) Ultrastructural evidence for the occurrence of three types of mechanosensitive cells in the tentacles of the cubozoan polyp Carybdea marsupialis. Protoplasma 173:13-22 Hausmann K, Holstein T (1985) Bilateral symmetry in the cnidocil-nematocyst complex of the freshwater medusa Craspedacusta sowerbii Lankester (Hydrozoa, Limnomedusae). J Ultrastruct Res 90: Holstein T (1981) The morphogenesis of nematocytes in Hydra and Forskalia: An ultrastructural study. J Ultrastruct Res 75: Holstein T, Hausmann K (1988) The cnidocil apparatus of hydrozoans: A progenitor of higher metazoan mechanoreceptors? In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, San Diego, pp Holstein T, Tardent P (1984) An ultrahigh-speed analysis of exocytosis: Nematocyst discharge. Science 223: Koizumi O, Wilson JD, Grimmelikhuijzen CJP, Westfall JA (1989) Ultrastructural localization of RFamide-like peptides in neuronal dense-cored vesicles in the peduncle of Hydra. J Exp Zool 249:17-22 Mariscal RN (1974) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology. Academic Press, New York, pp Slautterback DB (1967) The cnidoblastmusculo-epithelial cell complex in the tentacles of Hydra. Z Zellforsch 79: Stidwill RP, Honegger TG (1989) A single layer of microtubules is part of a complex cytoskeleton in mature nematocytes of Hydra. Tissue Cell 21: Stoessel F, Tardent P (1971) Die Reaktionsmuster von Coryne pintneri und Sarsia reesi (Athecata: Capitata) auf Ber/ihrungsreize. Rev Suisse Zool 78: Tardent P, Holstein T (1982) Morphology and morphodynamics of the stenotele nematocyst of Hydra attenuata Pall. (Hydrozoa, Cnidaria). Cell Tissue Res 224: Tardent P, Schmid V (1972) Ultrastructure of mechanoreceptors of the polyp Coryne pintneri (Hydrozoa, Athecata). Exp Cell Res 72: Weber J (1989) Nematocysts (stinging capsules of cnidaria) as Donnan-potential-dominated osmotic systems. Eur J Biochem 184: Westfall JA (1973) Ultrastructural evidence for a granule-containing sensory-motor-interneuron in Hydra littoraiis. J Ultrastruct Res 42: Westfall JA (1988) Presumed neuronematocyte synapses and possible pathways controlling discharge of a battery of nematocysts in Hydra. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, San Diego, pp Wood RL, Novak PL (1982) The anchoring of nematocysts and nematocytes in the tentacles of Hydra. J Ultrastruct Res 81 :
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