Ring-shaped organization of cytoskeletal F-actin associated with surface sensory receptors of Schistosoma mansoni: a confocal and electron microscopic study

The surface syncytial epithelium of the human blood fluke, Schistosoma mansoni, contains numerous ciliated or unciliated, bulb-shaped sensory receptors. At the ultrastructure level, sensory receptors with similar topographic and morphological structures have been found in the epithelial surface layers of all known species of schistosomes and other species of flatworm parasites. Although many studies have focused on the syncytial cytoskeleton of schistosomes, while some other studies have examined the fine structures of the syncytial sensory receptors, no-one has demonstrated the association of cytoskeletal elements with the surface sensory cells except the well-known microtubules associated with ciliated structures. The present study, using confocal laser scanning microscopy combined with scanning and transmission electron microscopies, demonstrates the association of ring-shaped F-actin within the epithelial sensory receptors. The F-actin rings can be characterized into two types according to their size, density, and distribution. The actin rings found in the syncytia of both the male and female schistosomes appear to be more dense and larger in size than the actin rings located only at the central regions of the tuberculated structures of the male dorsal syncytium. Our observation of F-actin rings associated with the spine-bearing tubercles, combined with the results obtained from other ultrastructural investigations, also indicate the presence of the unciliated sensory receptors in each tuberculated structure of the male dorsal surface syncytium, which have not been reported in other studies on schistosome epithelial sensory cells.     

Correlation of fluorescence and electron microscopy of F-actin-containing sensory cells in the epidermis of Convoluta pulchra (Platyhelminthes: Acoela)

Phalloidin‐stained whole mounts of acoel turbellarians show brightly fluorescing club‐shaped structures distributed over the epidermis and concentrated especially at the anterior and posterior tips of the body. By correlating electron micrographic images and fluorescence images of Convoluta pulchra, these structures can be seen to be sensory receptors with a central cilium surrounded by a collar of microvilli. The other candidate for showing fluorescence in the epidermis, namely gland necks, can be ruled out since their distribution is too dense to resemble the distribution of the fluorescent structures seen here. The collared sensory receptors were inserted between epidermal cells, and each bore a central cilium surrounded by a collar of 6–18 microvilli and an additional centrally positioned 2–7 microvilli of which 2 or 3 were associated with a modified rootlet called the swallow’s nest. Confocal scanning laser microscopy resolved the core of actin filaments within the microvilli of the collar and their rootlet‐like connections to the base of the sensory cell. Such receptors could also be identified by fluorescence microscopy in several other species of acoel turbellarians.     

The Nervous System of the Male Dinophilus gyrociliatus (Annelida: Polychaeta). I. Number, Types and Distribution Pattern of Sensory Cells

The entire nervous system of the smallest annelid hitherto known, the dwarf male of the highly dimorphic species Dinophilus gyrociliatus , has been reconstructed by means of TEM investigations of serial ultrathin sections. Altogether there are 68 neurons, 40 of which have a sensory function. The structure and distribution of them is described. The receptor endings of the 20 sensory cells of each side are located either in two groups — the anterior receptor group and the posterior receptor group — or are singly positioned in the integument. Structural differences of the apical portion of the dendrites enables four types of receptors to be distinguished: three types with emergent cilia and one type with non-emergent cilia. Neurons with emergent cilia can be monociliated collar cells as well as mono- or multiciliated cells without collar. Special vesicle-in-vesicle structures, are located close to the basal portion of the cilia in some of these cells. The non-emergent cilia border closely to a neighbouring epidermal cell and contain a prominent intraciliary vesicle. The function of receptors is discussed with regard to a comparison with receptors in other polychaete species, structural specializations and their distribution pattern on the animal's surface.     

Ultrastructure and chaetotaxy of sensory receptors in the cercaria of a species of Allopodocotyle Pritchard, 1966 (Digenea: Opecoelidae)

Previous investigations of sensory systems in opecoelid cercariae have focused on chaetotaxy and ultrastructure of sensory receptors. They revealed chaetotaxic patterns within family, genus, and species as well as different receptors. Chaetotaxic and ultrastructural observations have rarely been combined. We investigated the ultrastructure of cercarial sensory receptors in conjunction with chaetotaxy and neuromorphology in a species of Allopodocotyle. Cercariae were treated with acetylthiocholine iodide and silver nitrate, and some were processed for light, scanning (SEM), and transmission (TEM) electron microscopy. Five nerve regions were distinguished. Chaetotaxy was consistent with that of other opecoelids. Five types of receptors were distinguished with SEM. Types differed in number of cilium-like structures (one or more), length of cilium-like structure (short, moderately long, or long), presence or absence of a tegumentary collar, and length of tegumentary collar (low, moderately low, or very high). Internal ultrastructure of some types revealed unsheathed cilium-like structures, basal body, and thickened nerve collars. Possible subtegumentary and sheathed receptors are introduced. Some receptor types were site-specific. For example, receptors with multiple cilium-like structures were concentrated on cephalic region whereas receptors with short cilium-like structure were widespread throughout most regions. Ultrastructure and site-specificity observations suggest that most receptors are mechanoreceptors.     

Topography and ultrastructure of the tegument of Bucephalus anguillae (Digenea: Bucephalidae), a parasite of the European eel Anguilla anguilla (Osteichthyen: Anguillidae)

The tegumental ultrastructure of the intestinal fluke Bucephalus anguillae was studied with the use of scanning and transmission electron microscopy. The surface of the tegument is covered by transverse ridges from which protrude numerous closely packed, digitated, and claw-shaped spines. Cobblestone-like units of the tegument were observed on the crescent-shaped formation of the rhynchus and at the posterior part of the body. Three types of sensory structures were examined, i.e., 2 uniciliated receptors and 1 without cilia. As anterior-posterior differences were observed, particular attention was given to spines and sensory receptors. Spine insertion zones and average cilia length are variable between anterior and posterior tegument areas. Ultrastructural study revealed that the tegument of B. anguillae has a typical syncytial organization with a distal cytoplasm lying over a basal matrix and cytons below. Cytoplasmic bridges allowed transit of secretory vesicles and granules. Diagrams of spines and sensory receptors were made to help in understanding the nature of these structures.     

Identification and Pattern of Primary Sensory Cells in the Body Wall Epithelium of the Tubificid Worm, Limnodrilus hoffmeisteri

This study compares the effectiveness of two examination methods suitable for morphological observations, scanning electron microscopy (SEM) and light microscopic NADH-diaphorase (NADP-d) histochemistry, to identify location and distribution pattern of primary sensory cells situated in the body wall epithelium of Limnodrilus hofmeisteri. SEM observations revealed that grouped sensory cells forming two distinct types of sensillas (or sense organs) are scattered over the body surface. The easily identifiable first type (ciliated sensilla) contains numerous penetrative ciliate sensory cells while no ciliate sensory cells were seen in the second type (sensory bud). NADH-d staining proved to be a suitable method to identify both structures further staining solitary sensory cells, and certain sensory fibres that could not be visualised by SEM preparations. Our results show that NADH-d staining, as a histochemical marker of primary sensory cells, is a suitable and effective method to reveal their morphology and distribution pattern in whole mount preparations in the smallest detail, suggesting that the application of this relatively simple and cheap method may contribute to understand the basic organisation and evolution of the peripheral sensory structures of oligochaetes.     

Ultrastructure and chaetotaxy of sensory receptors in the cercariae of a species of Crepidostomum Braun, 1900 and Bunodera Railliet, 1896 (Digenea: Allocreadiidae)

Previous investigations of cercarial sensory systems have focused on chaetotaxy and ultrastructure of sensory receptors and have revealed chaetotaxic patterns within families, genera, and species as well as different types of sensory receptors. However, chaetotaxic and ultrastructural observations have rarely been combined. We investigated the ultrastructure of cercarial sensory receptors in conjunction with the chaetotaxy and neuromorphology in 2 allocreadiid species belonging to the genera Crepidostomum and Bunodera. Cercariae were treated with acetylthiocholine iodide and silver nitrate, and for scanning electron microscopy (SEM) and transmission electron microscopy (TEM). Similar cholinergic nerve networks were revealed. Chaetotaxy was consistent with that of other allocreadiids. Seven and 6 types of receptors were distinguished with SEM in Crepidostomum sp. and Bunodera sp., respectively. Types differed in number of cilia (1 or 2), cilium length (short, moderately long, or long), presence or absence of a tegumentary collar and a domelike base, and tegumentary collar length (low, moderately low, or high), TEM of some types revealed unsheathed cilia, basal body, and thickened nerve collars. Some receptor types were site specific. Thus, long uniciliated receptors were concentrated on the dorsal surface. Other types, such as short uniciliated receptors, were widespread throughout most regions. Ultrastructure and site-specificity observations suggest that most receptors are mechanoreceptors.     

Sensory cells in the sucker of Craspedella pedum (Plathelminthes, Temnocephalida): in vivo staining with DiO and SEM and TEM observations

 Two pairs of identified sensory neurons innervating the sucker of Craspedella pedum (designated ADS1, ADS2) were found to accumulate DiO (3,3′-dioctadecyloxacarbocyanine perchlorate) in vivo. The number, position and morphology of these neurons do not change throughout the postembryonic period of life. The axons of the ADS cells run forward within the ventral cords and their dendrites are parallel. They enter the sucker, ramify and terminate in numerous sensory endings in a wide peripheral zone of the disc. SEM reveals a single type of sensilla: small spot-like structures with several short cilia. They are scattered within the zone accommodating the openings of the adhesive glands and their distribution corresponds to that of the stained terminals. TEM observations (including about 20 full reconstructions from serial ultrathin sections) show five types of sensory endings on the disc with the following structures: (1) a short cilium and thin rootlet, (2) aciliary with a normal rootlet and a club-shaped apical portion, (3) aciliary with a club-shaped apical portion and a body similar to the apical part of the rootlet, (4) aciliary with large apical granule and (5) aciliary with small apical granules. Type 2–5 receptors form a morphological series suggesting that they are stages of formation of the common type 4 receptor. Not fully formed type 1 receptors have been found within the epidermis in adult animals. This suggests that, although ADS perikarya persist throughout the life of the animal, the nerve endings they form might be constantly renewed. Judging from the morphological and behavioural data, the functions of the ADS neurons might include: (1) monitoring of the close contact between the surface of the sucker and the substratum prior to adhesion and (2) checking the viscosity of the adhesive secretion prior to release of the sucker. Accepted: 16 December 1997     

External sense receptors in microdrile oligochaetes (Annelida,Clitellata) as revealed by scanning electron microscopy: Typology and patterns of distribution in the main taxonomic groups

This work summarizes the observations on 30 species of microdriles belonging to the families Naididae (Rhyacodrilinae, Pristininae, Naidinae, Phallodrilinae, and Tubificinae), Phreodrilidae, Lumbriculidae, and Enchytraeidae using scanning electron microscopy. The lumbricid Eiseniella tetraedra, a megadrile species common in typical microdrile habitats, was used for comparison. Microdriles display external ciliate sense structures along the entire body; even at the clitellum and in budding and regeneration zones. According to the shape of the cilia, these sense structures can be divided into receptors of blunt cilia, receptors of sharp cilia, and composed receptors. Sense receptors can be morphologically unconspicuous or clearly defined on sensory buds or papillae. All microdriles studied have receptors of blunt cilia. Enchytraeids have characteristic receptors of short cilia. Pristina (Pristininae), Chaetogaster, Ophidonais, and Stylaria (Naidinae) have receptors of long blunt cilia. Composed receptors were found only in some microdriles and E. tetraedra. Receptors of sharp cilia have been found in most microdriles. Enchytraeids might be the only exception, but sharp cilia are probably present in the amphibiotic Cognettia sphagnetorum. Sensory cells with long sharp cilia might play a rheoreceptor role, and their presence in E. tetraedra and C. sphagnetorum would imply the reappearing of an ancient character that was probably lost with the transit from aquatic to terrestrial habitats. Some lumbriculids have ciliated fields. Anatomically, these structures appear as intermediate between the typical isolate sensory structures of microdriles and the sensillae of the hirudineans. The general pattern in microdriles is that uniciliate receptors and multiciliate receptors are separated, which supports the presumed aquatic origin of the clitellates. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Description and surface topography of the cercaria of Austrobilharzia sp. (Digenea: Schistosomatidae)

The cercaria of Austrobilharzia sp. from the marine prosobranch gastropod Planaxis sulcatus in Kuwait Bay is described. The surface microtopography and pattern of the tegumentary sensory receptors are examined using scanning electron microscopy. The general microtopography of the surface of the cercaria is similar to that previously observed in cercariae of mammalian schistosomes, although differences are recorded in the types, numbers and distribution of the sensory receptors. The study identified more than 13 types of receptors comprising aciliated, uniciliated and for the first time a multiciliated receptor in a strigeid cercaria. The ciliated receptor types differ in the cilium length and structure of the surrounding collar and tegumentary base. The receptor types are site specific: (1) the aciliated and pitlike on the anterior organ-neck region and ventral sucker; (2) the uniciliated with a long flexible cilium with or without collar or a tegumentary base on the body and tail; and (3) the uniciliated with a short rigid cilium and a robust collar and tegumentary base, and the multiciliated with 6 flexible cilia and a high cylindrical collar on the anterior organ tip. The reported SEM information on the sensory receptors may contribute to elucidating their functional role and to establishing morphological characters for the phylogeny of the family Schistosomatidae.     

Tissue distribution of the opioid receptor-like (ORL1) receptor

The ORL1 receptor is a G protein-coupled receptor structurally related to the opioid receptors, whose endogenous ligand is the heptadecapeptide nociceptin/orphanin FQ. In this review, data which have contributed to the mapping of the anatomic distribution of the ORL1 receptor have been collated with an emphasis on their relation to physiological functions. The ORL1 receptor is widely expressed in the central nervous system, in particular in the forebrain (cortical areas, olfactory regions, limbic structures, thalamus), throughout the brainstem (central periaqueductal gray, substantia nigra, several sensory and motor nuclei), and in both the dorsal and ventral horns of the spinal cord. Regions almost devoid of ORL1 receptors are the caudate-putamen and the cerebellum. ORL1 mRNA and binding sites exhibit approximately the same distribution pattern, indicating that the ORL1 receptor is located on local neuronal circuits. The ORL1 receptor is also expressed at the periphery in smooth muscles, peripheral ganglia, and the immune system. The anatomic distribution of ORL1 receptor suggests a broad spectrum of action for the nociceptin/orphanin FQ system (sensory perception, memory process, emotional behavior, etc.).     

Sensory receptors of the rosette organ of Gyrocotyle rugosa

The fine structure of three sensory receptors of the rosette organ of Gyrocotyle rugosa, is described. The Type I sensory receptors, localised towards the edge of both upper and lower surfaces, are characterized by a long cilium embedded in a bulb containing two electron-dense collars and several mitochondria. The Type II sensory receptors, larger than Type I, are located on the upper surface of the rosette and have a long cilium and a ciliary rootlet. They also have two electron-dense collars and one or two mitochondria. The sensory cilia of both types are characterized by 9 + 2 axonemes. The Type III sensory receptors, localised on the under surface, lack a sensory cilium but have a ciliary rootlet and are enclosed in the tegument and musculature; there is a complicated three-dimensional spherical lattice of microfibrils associated with the rootlet. The sensory bulbs contain large numbers of membrane bound vesicles and neurotubules. A function is postulated for each of the three types of sensory receptors.     

Ribeiroia marini: Surface ultrastructure of redia,cercaria, and adult

Rediae, cercariae, and adults of Ribeiroia marini were examined using a scanning electron microscope to determine the types of tegumental sensory structures and their locations. Sensory structures were observed among numerous tegumental folds in the area immediately surrounding the mouth of the rediae. These sensory structures are similar in appearance, location and fine structure to sensory structures described from the anterior tips of rediae known to be predacious on the sporocysts of Schistosoma mansoni. These uniciliated structures may function as chemoreceptors to aid the redia in migration through snail tissue. Five types of sensory structures bearing one, two, or multiple cilia were distinguishable on the cercariae. These structures were located on and around the oral sucker, dorsal and ventral body surfaces and on the tail. They may be used by the cercariae to locate the intermediate host fish and to find suitable sites within the lateral line scales for encystment. The ventral surface of the adult fluke is covered with spines and shows an absence of sensory structures on the general body surface. Sensory structures were seen in the area surrounding the oral and ventral suckers. The extended cirrus organ has a folded tegument, but lacks spines or sensory structures.     

Three-dimensional fine structural reconstruction of the nose sensory structures of Acrobeles complexus compared to Caenorhabditis elegans (Nematoda: Rhabditida)

Nematode sensory structures can be divided into two classes; cuticular sensillae, with dendrites ending outside the epidermis, and internal receptors, that typically are single dendrites terminating within the body cavity. Fine structure of the former has been described completely in more than a dozen nematode taxa, while the latter were previously only well understood in the microbial feeder Caenorhabditis elegans. The distantly related nematode Acrobeles complexus has a similar ecology and together the two span a clade representing a large proportion of nematode biodiversity. The cuticular sensillae and internal receptors of A. complexus are here shown to be remarkably similar in number, arrangement, and morphology to those of C. elegans. Several key differences are reported that likely relate to function, and suggest that this nematode has a cuticular sensillum morphology that is closer to that of the common ancestor of the two taxa. Internal sensory receptors have more elaborate termini than those of C. elegans. The existence of a novel form of mechanoreceptor in A. complexus and spatial relationships between sensillum dendrites suggest differences between two classes of sensillae in how a touch-response behavior may be mediated.     

Podial sensory receptors and the induction of metamorphosis in echinoids

Larvae of Strongylocentrotus droebachiensis (Müller), Lytechinus pictus (Verrill), and Lytechinus variegatus (Leske) which are competent to metamorphose display what appears to be substratum-testing behavior prior to metamorphosis. Larvae cease swimming, partially evert the adult rudiment, and walk about examining the substratum with their five primary podia. Larvae eithe r metamorphose or withdraw their podia and resume swimming to settle again elsewhere. Scanning and transmission electron microscopic examinations of the primary podia revealed sensory receptor cells on the rim and on a conical projection at the center of the podial sucker. Each sensory cell has a single short cilium on its apical surface a axonal process at its base which contributes to the basiepithelial nerve plexus. Mature adults of the same species also have comparable sensory structures on their tube feet suckers. It is suggested that the sensory receptors on the primary podia of setting larvae, although they are not specialized larval structures, may be involved in the perception of tactil e stimuli which have been previously demonstrated to be involved in the induction of metamorphosis.     

Neurochemical characterization of nervous elements innervating the body wall of earthworms (Lumbricus, Eisenia): immunohistochemical and pharmacological studies

The distribution and chemical neuroanatomy of nervous elements and certain pharmacological–physiological characteristics of the innervation of the body wall in earthworms are described. Solitary sensory bipolar cells can be found among the epithelial cells. These bipolar cells contain serotonin, tyrosine hydroxylase, histamine, gamma-amino-butyric acid (GABA), Eisenia tetradecapeptide, proctolin or rhodopsin in various combinations. In the body wall, the plexus submuscularis is composed of nerve fibres only, whereas the plexus subepithelialis and muscularis also contain solitary nerve cells. These cells display histamine, GABA or neuropeptide Y immunoreactivity. The fibres of the three plexuses are reactive to serotonin, histamine, Eisenia tetradecapeptide, proctolin, GABA and neuropeptide Y antibodies. FMRFamide-immunoreactive fibres of the plexus muscularis originate from the central nervous system, whereas axons containing the other studied molecules are derived from both peripheral and central structures. High pressure liquid chromatography assays have revealed serotonin, dopamine and histamine in the body wall. Contractions of the body wall musculature can be elicited with serotonin and FMRFamide. Serotonin-evoked contractions are suppressed by the application of GABA. Serotonin acts both directly on the muscle cell receptors and indirectly through initiating transmitter release from the nervous elements, whereas the FMRFamide-induced contractions seem to be mediated through the muscle cell receptors only. The pharmacological profiles of the serotonin and GABA receptors resemble those of the vertebrate 5-HT₃ and GABA_B receptor types. Our findings indicate that both the sensory and efferent system of the annelid body wall operate by means of a variety of neuroactive compounds, suggesting a complex role of signalling systems in the regulation of this organ.This work was supported by the Hungarian Scientific Research Fund (OTKA; grant nos. T 34106 and T 34160). Márta Wilhelm is in receipt of a János Bolyai Scholarship.     

Ultrastructure of epidermal sensory receptors in Amphibolurus barbatus (Lacertilis: Agamidae)

Summary The histological and ultrastructural organisation of the epidermal sensory organs in Amphibolurus barbatus has been described with respect to their position and possible functions. The sensory organs, located at the scale's edge, are most numerous in scales of the dorsal surface of the head. Most other scales of the body surface have two receptors located laterally to the spine or keel of the scale. In the imbricate scales of the ventral body region, the receptors lie just beneath the reinforced scale lip. Scanning electron microscopy has revealed the surface of the organ to be a crater lacking any surface projections. These sensory organs have a dermal papilla consisting of a nerve plexus and loose connective tissue. The nerve fibres arising from the plexus, pass to the epidermal columnar cells, where some form nerve terminals at the base of the cells, while others pass between them to form nerve terminals embedded in a superficial layer of cuboidal cells. The superficial terminals are held against the overlying keratin by masses of tonofilaments. The keratin is thickened to form a collar around the periphery of the organ but is only about 0.5 m thick immediately above it. Mechanical deformation of the scale's spine or reinforced scale lip may initiate stimulation of the nerve terminals described.     

Structural Organization of the Taste Apparatus in Characins (Characidae,Teleostei)

The morphology and distribution of taste buds in the outer integument of the body and in the oral cavity of two forms (blind cave and sighted terrestrial ones) of the astyanax Astyanax fasciatus and in intact and blinded individuals of the Buenos Aires tetra Hyphessobrycon anisitsi have been studied using electronic scanning and light microscopy. In sighted individuals of both species, the morphometric parameters of the taste apparatus and the distribution of taste receptors are similar; the taste apparatus in the oral cavity is more developed than in the outer covers. Morphologically different taste zones were found in the oral cavity of characins. In blind fish, the taste apparatus of the maxillary zones is distinguished by smaller taste buds and a greater density of their distribution. The sensory field of taste buds in blind and sighted individuals of astyanax and tetra has a similar ultrastructure; it is formed by taste cells of three types. In blind astyanaxes and blinded individuals of tetra, numerous modified epidermal cells were found for the first time in the epithelium of the taste zones and in contact with taste buds, which are regarded as tactile receptors and a constituent element of polysensory taste-tactile complexes localized in blind fish in mainly ventral sensory zones.     

Cell surface adhesion receptors

Several new structural motifs found in cell surface adhesion receptors have been described in the past few years. Also, several two-domain structures of extracellular portions of cell surface proteins have been reported. Structural models for complexes between receptors and counter-receptors have been proposed. The first reports on carbohydrate conformation in intact glycoprotein domains have recently appeared. These new data are presented within a more general review of the field of cell adhesion receptors.