cestoda: anoplocephalidae - BioOne

J. Parasitol., 92(5), 2006, pp. 953–961 䉷 American Society of Parasitologists 2006

CELLULAR ORGANIZATION OF THE ONCOSPHERE OF MOSGOVOYIA CTENOIDES (CESTODA: ANOPLOCEPHALIDAE) Daniel Młocicki*†, Zdzisław S´widerski*‡, Jordi Miquel§, Catarina Eira§, and David Bruce Conn㛳 * W. Stefan´ski Institute of Parasitology, Polish Academy of Sciences, 51/55 Twarda Str., 00-818 Warsaw, Poland. e-mail: [email protected] ABSTRACT: The ultrastructure of the infective oncosphere of the cestode Mosgovoyia ctenoides (Anoplocephalidae) is described. The surface of the infective oncosphere is covered by a thin cytoplasmic layer of tegument connected by a narrow cytoplasmic process with the binucleate subtegumental cell, situated deeper in the body. Below the basal matrix of the cytoplasmic layer of the tegument are situated wide bands of the peripheral, somatic musculature responsible for body movements. The 3 pairs of hooks and their muscles form a complex hook muscle system, responsible for coordinated hook action. Five major types of cells have been distinguished: (1) a binucleate subtegumental cell, (2) a binucleate penetration gland, (3) 2 nerve cells, (4) numerous somatic cells, and (5) about 6 germinative cells. The approximate number of cells is 24 (26 nuclei, including 2 syncytial structures). The results of this study, when compared with other published reports from other cestode taxa, support previous hypotheses that the progressive reduction of oncosphere cells is an adaptive feature in cestode evolution.

RESULTS

The Anoplocephalidae includes cestodes parasitic in different groups of vertebrates, including humans, common throughout the world (Beveridge, 1994). A better knowledge of the infective larval stages of anoplocephalid cestodes, which develop into metacestodes in oribatid mite intermediate hosts, is important to understanding the epidemiology of these worms. As adults, species of Mosgovoyia Spasskii, 1951 are frequently parasites of leporid lagomorphs, and rarely rodents in Europe, Africa, Asia, and North and South America. As reported recently (Gundłach and Sadzikowski, 2004), Mosgovoyia ctenoides (Railliet, 1890) Beveridge, 1978, is a very common parasite of domestic and wild rabbits and sometimes also hares; thus, it may have an economic impact. The purpose of the present study was to describe the ultrastructure of mature oncospheres of the anoplocephalid cestode M. ctenoides, with particular emphasis on the cellular organization on the hexacanth and structures directly involved in the mechanism by which it infects the intermediate host.

The schematic diagram (Fig. 1) shows the general topography and bilateral symmetry in cellular organization of the infective larvae, which are usually ovoid and measure approximately 30 ␮m (Fig. 2). With regard to oncosphere terminology, we follow that proposed by Ogren (1971). Such terms as ‘‘anterior pole’’ and ‘‘posterior pole’’ of the oncosphere are used in this article with respect to hexacanth invasive activity. Larvae use hooks, generally in conjunction with penetration gland secretion, to penetrate through host tissue with the hooks oriented in the direction of movement. Therefore, the hook region, directed forward during movement, is considered as the anterior part of the larvae and functionally as the ‘‘somatophore.’’ The opposite hemisphere, containing germinative cells, is considered as posterior and functionally as ‘‘germatophore’’ or ‘‘mesophore.’’ The mature hexacanth is armed with 3 pairs of hooks, 1 medial pair and 2 lateral pairs (Figs. 1, 2), interconnected by a complex hook muscle system (Figs. 3, 7A) responsible for coordination of their synchronized movements. The fully formed hooks at oblique and cross sections seem to have a heterogeneous structure and are composed of 2 or 3 layers of different electron densities (compare Figs. 3, inset and 6C). In M. ctenoides, the infective oncosphere consists of about 24 symmetrically arranged cells, including 2 binucleate structures, namely, the penetration gland and the tegumental perikaryon (also known as the ‘‘binucleated subtegumental cell’’). Five major cell types were distinguished: (1) a binucleate subtegumental cell; (2) a binucleate penetration gland; (3) 2 nerve cells; (4) about 14 small somatic cells, which represent myocytons of somatic and hook musculature; and (5) 6 large germinative cells. A thin anucleated layer of tegument (Fig. 4A) covers the hook region of the oncosphere. It possesses characteristic long tegumental processes at the anterior pole (Fig. 4C). This anucleated tegumental component is connected by a narrow cytoplasmic process with a binucleate tegumental perikaryon (Fig. 4B), situated deeper in the body below the hook bases. This syncytial cell is characterized by the presence of 2 closely adjacent large spherical nuclei, both containing large electrondense nucleoli. Below the basal matrix of the cytoplasmic layer of the tegument are situated wide bands of the peripheral, somatic musculature responsible for body movements (Fig. 4A). The penetration gland forms a U-shaped, binucleate syncytium with 2 arms that open into the tegumental peripheral layer

MATERIALS AND METHODS Adult specimens of M. ctenoides (Railliet, 1890) Beveridge, 1978, were obtained from the small intestine of naturally infected wild rabbits (Oryctolagus cuniculus) collected in Quiaios, Portugal. The cestodes were isolated from the intestine, washed in saline, and cut into small pieces. Tissue samples of mature and gravid proglottids were fixed for 2 hr in cold 2% glutaraldehyde in 0.1 M cacodylate buffer, pH 7.2, washed in the same buffer, and postfixed in 1% OsO4 for 2 hr. Material was dehydrated in a graded ethanol series and propylene oxide and embedded in Spurr’s epoxy resin. The consecutive semithin serial sections, stained with 1% methylene blue in borax solution, were used to construct a schematic diagram of the oncosphere. Ultrathin serial sections, double stained with uranyl acetate and lead citrate, were examined under a JEM 100 B transmission electron microscope (TEM) operated at an accelerating voltage of 80 kV.

Received 21 November 2005; revised 1 February 2006, 14 March 2006; accepted 14 March 2006. † Department of Medical Biology, Medical University of Warsaw, 73 Nowogrodzka Str., 02-018 Warsaw, Poland. ‡ Department of General Biology and Parasitology, Medical University of Warsaw, 5 Chałubin´skiego Str., 02-004 Warsaw, Poland. § Laboratori de Parasitologia, Facultat de Farma`cia, Universitat de Barcelona, Av. Joan XXIII s/n, E-08028 Barcelona, Spain. 㛳 To whom correspondence should be addressed. School of Mathematical and Natural Sciences, Berry College, Mount Berry, Georgia 30149-5036. 953

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THE JOURNAL OF PARASITOLOGY, VOL. 92, NO. 5, OCTOBER 2006

FIGURE 1. Schematic diagram illustrating the internal organization and bilateral symmetry in the cellular organization of the oncospheres of M. ctenoides. BSC, binucleated subtegumental cell; HRM, hook-region membrane; GC, germinative cells; NC, nerve cells; OT, oncosphere tegument; PG, penetration gland; SC, somatic cells.

by gland exits located between the medial and lateral hook pairs (Fig. 1). The nuclei of the fully developed gland are irregular in shape and contain several heterochromatin islands (Figs. 3, 5A). They are surrounded by a granular syncytial cytoplasm, rich in free ribosomes, well-developed granular endoplasmic reticulum (GER), numerous mitochondria (Figs. 3, 5A), and characteristic, flattened, discoidal secretory granules, frequently grouped in assemblages including 3 to 6 granules (Fig. 5B). The nerve cells are situated at the central part of the oncosphere in the penetration gland invagination (Fig. 1). The nuclei of these cells contain large osmiophilic heterochromatin islands usually adjacent to the nuclear membrane (Fig. 6A). Moreover, nerve cells are characterized by the presence of membranebound, dense-cored neurosecretorylike granules in their cytoplasm (Fig. 6A). In addition to their presence in the perikarya, the typical neurosecretory granules also were observed in the elongated nerve processes (Fig. 6A, B), frequently adjacent to the body and hook–muscle system (Fig. 6C). Somatic cells represent the myocytons of somatic and hook

musculature (Figs. 2, 3, 7A, C). They are situated mainly in the anterior of the infective larvae. Somatic cells are frequently characterized by the connection with long muscle fibers (Fig. 7C). They contain oval or spherical nuclei rich in the heterochromatin islands that are dispersed in the karyoplasm, and large electron-dense nucleoli. The rather thin layer of cytoplasm surrounds the nuclei. However, somatic cells are always smaller and their nucleocytoplasmic ratio is lower than in the germinative cells. The large germinative cells are localized in the posterior pole, near a deep invagination of the U-shaped penetration gland (Figs. 1–3). They are arranged symmetrically in 2 groups of 3 large cells (Figs. 1, 2). These cells, showing a high nucleocytoplasmic ratio, are characterized by the presence of large, lobate granular nuclei containing prominent electrondense, spherical nucleoli surrounded by numerous irregular heterochromatin islands adjacent to the nuclear membrane (Fig. 7B). The very thin granular layer of cytoplasm of these cells is rich in free ribosomes (Fig. 7B).

MŁOCICKI ET AL.—CELLULAR ORGANIZATION OF MOSGOVOYIA ONCOSPHERES

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FIGURE 2. Cross section of the infective oncosphere showing localization of germinative (GC) and somatic (SC) cells in relation to the hooks (H) as anterior pole of the hexacanth embryo, and penetration gland (PG) as posterior pole. Note the thin layer of oncosphere tegument (OT) covering the larval body at the hook region and 3 pairs of hooks (H). sg, secretory granules; SM, somatic musculature.

DISCUSSION The ultrastructural data available so far on the cellular organization of the infective oncospheres of anoplocephalid cestodes are limited to 2 species, Anoplocephaloides dentata (reported by S´widerski et al., 2001) and Inermicapsifer madagascariensis (S´widerski and Tkach, 2002). The results of the present TEM study revealed that the general ultrastructure and cellular components of the hexacanth larvae of M. ctenoides are similar to those observed in other cyclophyllidean families (for references, see Ogren, 1968a, 1968b; Rybicka, 1964; Collin, 1969; S´widerski, 1972, 1981, 1983; S´widerski and Tkach, 1997a, 1997b, 1999; Tkach and S´widerski, 1997). The thin layer of oncosphere tegument (the so-called ‘‘embryonic epithelium’’ of Rybicka, 1972), covers only the hookregion pole of the oncosphere of M. ctenoides. This area, including the hook blades and oncosphere tegument, is surrounded by the hook-region membrane (Młocicki, S´widerski, Miquel, and Eira, 2005). The hook-region membrane also was described by S´widerski et al. (2001) and by S´widerski and Tkach (2002) in 2 other anoplocephalids, A. dentata and I. madagascariensis. Similar ultrastructure of the oncosphere tegument was reported in the representatives of other families of cestodes (Rybicka, 1973; Ubelaker, 1983; S´widerski, 1995; S´widerski and Tkach,

1997a, 1997b, 1999, 2002; Tkach and S´widerski, 1997; S´widerski et al., 2000; S´widerski and Mackiewicz, 2004). All these studies confirm that the tegument is composed of 2 components: an anucleated distal cytoplasmic layer connected by a narrow cytoplasmic bridge to its perikaryon. It shows some similarity to the tegumental composition of adult M. ctenoides (Młocicki et al., 2004). The only different interpretation of the oncosphere tegument was proposed by Korneva (1994) who described unusual features of it in Triaenophorus nodulosus. Korneva claimed that the cytoplasmic layer of the tegument is formed by a single cell, the nucleus of which remains in this layer even in the infective oncosphere of this species. It is important to note that the marked difference between the tegument of oncospheres and that of metacestodes and adults is a primary feature distinguishing larval and postlarval stages in cestodes (Conn, 2005). The numerous tegumental processes (similar to microvilli) were distinguished in the oncosphere of M. ctenoides, whereas they seem to be absent from the hexacanths of 2 other anoplocephalids examined so far (S´widerski et al., 2001; S´widerski and Tkach, 2002). Such tegumental processes also were reported in the oncospheres of Taenia taeniaeformis by Nieland (1968); Hymenolepis citelli by Collin (1968); Hymenolepis nana by Furukawa et al. (1977); H. diminuta by Lethbridge

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FIGURE 3. Part of the oncosphere showing the penetration gland (PG) containing numerous mitochondria (m) and secretory granules (sg); small somatic cells (SC) or myocytons of hook (HM) and somatic musculature; and several large germinative cells (GC). Inset, cross section through the oncosphere hook (H). Note the 3 layers of hook material.

FIGURE 4. Two components of the oncosphere tegument (OT). (A, C) The peripheral, anucleated, cytoplasmic layer with long tegumental processes (LP). (B) Binucleate subtegumental cell (BSC). CB, cytoplasmic bridge; lsg, large spherical secretorylike granules; SM, somatic musculature.

(1980); 2 Dilepididae, Anomotaenia constricta and Paricterotaenia porosa, by Gabrion (1981); and another dilepidid, Hepatocestus hepaticus, by S´widerski et al. (2000). The functions of the oncosphere tegument processes still remain unknown; however, they may have a function similar to that of the tegument of adult tapeworms. The presence of long processes greatly extends the surface area of the hexacanth embryo (Lethbridge, 1980) in the hook region; therefore, they are probably involved in the increase of absorptive surface important for transport of nutrients and other substances. Despite that the formation of the tegument has not been examined in detail, our observations on its development (Młocicki, S´widerski, Miquel, and Eira, unpubl. obs.) and ultrastructural organization in infective oncospheres suggest that its pattern of differentiation is similar to that described by Rybicka (1973) for H. diminuta and by S´widerski (1992, 1995), respectively, for Oochoristica agamae and Echinococcus granulosus. The penetration gland of M. ctenoides is similar to the Ushaped syncytial glands described previously in other cyclophyllideans by Ogren (1968a), Nieland (1968), Collin (1969), Pence (1970), Lethbridge and Gijsbers (1974), Furukawa et al. (1977), Lethbridge (1980), S´widerski (1982, 1986), Ubelaker (1983), S´widerski and Tkach (1997a, 1999, 2002), Tkach and


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FIGURE 5. (A) High-power magnification showing ultrastructural details of the penetration gland (PG) containing large nucleus (N) with numerous heterochromatin islands dispersed in nucleoplasm, and profiles of granular endoplasmic reticulum (GER) in their dense, ribosome-rich granular cytoplasm. (B) Characteristic discoid secretory granules (sg), frequently forming stacks.

S´widerski (1997), and S´widerski et al. (2001). In the previous light (LM) and electron microscopic studies of other cestode species, the penetration gland was described as binucleated (S´widerski, 1982; S´widerski and Tkach, 1997a, 1999; S´widerski et al., 2001), 4-nucleated, 6-nucleated (S´widerski and Tkach, 2002), multicellular (Chew, 1983), or unicellular (S´widerski, 1982; S´widerski and Tkach, 1997a, 1999, 2002; S´widerski et al., 2001). The mechanism of penetration gland secretion has been classified as merocrine, apocrine, or holocrine (for reviews, see Lethbridge, 1980; S´widerski and Tkach, 1997a, 1997b). Among anoplocephalids examined by LM and electron microscopy, the penetration glands were described in only 3 species, i.e., Moniezia expansa, A. dentata, I. madagascariensis. In LM studies, the penetration gland in M. expansa was initially described by Sinitsin (1931) as a typical binucleated syncytial gland, but Rybicka (1964) claimed that there are 2 separate penetration glands in the same species. In TEM studies S´widerski and Tkach (2002) showed that I. madagascariensis is unique in having a 6-nucleated penetration gland. In another anoplocephalid examined by TEM, A. dentata, the penetration gland also possesses the U-shaped binucleated structure. The secretory granules of the penetration gland, the accumulation of which fills most of the gland cytoplasm of A. dentata and I. madagascariensis, greatly resemble those of M. ctenoides. Those granules in all 3 species represent the electron-dense biconcave discs, which are tightly packed, and in some regions form parallel stacks or similar assemblages. A second type, less electron-dense and with larger vesicles, may represent a transitional stage. The precise chemical nature of the penetration gland secretion in M. ctenoides has yet to be established. In previously published articles on this subject, it has been described variously as proteinaceous substance with presumed enzymatic properties (Pence, 1970; S´widerski, 1972, 1982; S´widerski and Tkach, 1997a, 1997b, 1999, 2002); a polysaccharide complex, resistant or not, to amylase digestion (Sawada, 1961; Pence, 1970; S´widerski, 1972; Fairweather and Threadgold,

1981); or an acid mucopolysaccharide (Heath, 1971). The possibility that the gland produces more than 1 type of secretory material was suggested in LM studies by Sawada (1961). At the TEM level, the occurrence of 2 morphologically distinct types of secretory granules has been described in numerous cestode species, and they may be chemically and functionally distinct (Collin, 1969; Pence, 1970; S´widerski, 1972, 1982; Lethbridge and Gijsbers, 1974; Fairweather and Threadgold, 1981; S´widerski and Tkach, 1997a, 1997b, 1999, 2002). As mentioned above, the intermediate or transitional stages between the 2 types have been observed frequently; the granules may have similar chemical composition and simply represent changes due to their maturation, liquefaction, structural changes, or a combination, before secretion. Similar to the results reported by Lethbridge and Gijsbers (1974) for H. diminuta, M. ctenoides also forms large spherical granules are; however, in M. ctenoides formation of these characteristic blebs occurs when the oncosphere is still situated inside the uterus, which may suggest an apocrine character of the penetration gland secretion in M. ctenoides. The precise mechanism of oncosphere penetration into a host remains to be elucidated. The assumption that the penetration gland functions in penetration is based on 3 arguments: (1) the time when the secretory vesicles are expelled during penetration; (2) depletion, namely, the reduction or exhaustion of gland contents; and (3) destruction of intermediate host tissue (Fairweather and Threadgold, 1981). The lysis of host tissue in the vicinity of the invading oncospheres was demonstrated by Heath (1971) and Moczon (1977). Our results and arguments presented above from the literature suggest that in the oncosphere of M. ctenoides, the penetration gland secretion together with hook action plays an important role in the mechanism of intermediate host infection. In the oncospheres of M. ctenoides, as in most of other cyclophyllideans, 2 nerve cells were observed, localized in the invagination of the penetration gland. The identification is based on the presence of the characteristic granules of neuro-

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FIGURE 6. (A) Oncosphere nerve cells (NC) under high magnification showing the presence of numerous characteristic neurosecretory granules (nsg) in their cytoplasm. (B) Nerve processes (NP) filled with the neurosecretory granules (nsg). (C) The nsg originating from neurons and distinguished in the neurons and nerve fibrils near the hook (H). Note 2 layers of hook material of different electron densities. Hch, heterochromatin islands; N, nuclei of nerve cells; SC, nucleus of somatic cell; SM, somatic musculature.


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FIGURE 7. (A) Ultrastructural details of the somatic cells (SC) as myocytons of hook (HM) musculature. (B) Large germinative cell (GC). Note the following characteristics of germinative cells: a high nucleocytoplasmic ratio; large lobate nucleus (N) containing prominent electrondense nucleolus (n) and several heterochromatin islands; and a very thin layer of granular cytoplasm rich in free ribosomes. (C) Note the myocyton (SC) of the somatic musculature (SM) with long processes of muscle bundles. H, oncosphere hooks.

secretory types observed in nerve cell cytoplasm and inside the elongated nerve processes. Their ultrastructure corresponds to a cell type previously described by Fairweather and Threadgold (1981), S´widerski (1983, 1986, 1997), S´widerski and Tkach (1997a, 1997b), Tkach and S´widerski (1997), and S´widerski and Mackiewicz (2004). Such cells also were observed in 2 other anoplocephalid species examined by TEM, A. dentata by S´widerski et al. (2001) and in I. madagascariensis by S´widerski and Tkach (2002). The results of this study and previously published data (Młocicki, S´widerski, Conn et al., 2005) show the presence of neurosecretory granules near the hook and somatic musculature as well as near the penetration gland, which may confirm their important function in coordination of hook and body movements and also secretory activity of the penetration gland. S´widerski et al. (2001), stressed that classification of those cells into a neurosecretory type, as emphasized by Fairweather and Threadgold (1981), was based on purely cytological criteria; additional information is needed to confirm this viewpoint and to better understand their function. We emphasize, however, that in the oncospheres of some species, e.g., Catenotaenia pusilla (reported by S´widerski, 1972) and Hepatocestus hepaticus (reported by S´widerski et al., 2000), the nerve cells were absent. Somatic and germinative cells are 2 main cell types of the infective larvae and are symmetrically distributed in the hexacanth embryo. As in other cyclophyllidean oncospheres (for review, see S´widerski and Tkach, 2002), the most numerous are the somatic cells, which represent the myocytons of both hook

and somatic musculature responsible for coordinated hook and body movements. They are evidently smaller than germinative cells, and their number is about 14. The number of germinative cells in M. ctenoides is 6, as it is in A. dentata, whereas the oncospheres of I. madagascariensis contain about 12 germinative cells. The germinative cells in the oncospheres of 3 anoplocephalids examined by means of TEM show evident interspecific differences in their ultrastructural details; in I. madagascariensis and in M. ctenoides, their nuclei are very large and lobate, whereas in A. dentata they are smaller, always have a smooth surface, are oval or elongate, and lack predominant nucleoli. Both nuclear and cytoplasmic ultrastructural characteristics of germinative cells indicate their great developmental potential for further growth and postembryonic multiplication (S´widerski et al., 2002). As shown in our results, the approximate number of cells in the infective oncospheres of M. ctenoides is 24 (26 nuclei), including 2 syncytial structures, the binucleate tegumental perikaryon, and binucleate penetration gland. A different number of oncosphere cells was reported in 2 other anoplocephalids examined by TEM, e.g., I. madagascariensis, where according to S´widerski and Tkach (2002), the number of cells is 44 (50 nuclei), and A. dentata, where 26 cells (28 nuclei) occur (S´widerski et al., 2001). In an LM study on M. expansa, Rybicka (1964) reported the presence of only 15 cells, including 2 penetration glands. It is possible that the discrepancy in the cell number between representatives of different anoplocephalid genera examined by means of LM and TEM also derives from

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the different limits of resolution and other methodological differences. According to S´widerski (1983), the number of cells is one of the main differences between the oncospheres of different cestode orders. The comparison of the number of about 160 cells in pseudophyllideans (S´widerski and Mackiewicz, 2004); between 70 and 80 in proteocephalans (S´widerski, 1981); and much lower, but greatly variable, numbers in cyclophyllideans, i.e., between 5 and 52 cells (compare Collin, 1969; S´widerski, 1983, 1972; S´widerski and Tkach, 1997a, 1997b, 2002, 1999; S´widerski et al., 2001) supports previous hypotheses (S´widerski, 1983) that the progressive reduction in number of cells is an adaptive feature in cestode evolution. ACKNOWLEDGMENTS We thank the ‘‘Serveis Cientı´fics i Te`cnics’’ of the University of Barcelona for support in the preparation of samples. This work was funded by the Polish Ministry of Education and Science Grant 2P04C 121 29. The study was partially financed by the ‘‘DURSI (Generalitat de Catalunya).’’

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