The tapeworm interactome: inferring confidence scored protein-protein interactions from the proteome of Hymenolepis microstoma.

BACKGROUND: Reference genome and transcriptome assemblies of helminths have reached a level of completion whereby secondary analyses that rely on accurate gene estimation or syntenic relationships can be now conducted with a high level of confidence. Recent public release of the v.3 assembly of the mouse bile-duct tapeworm, Hymenolepis microstoma, provides chromosome-level characterisation of the genome and a stabilised set of protein coding gene models underpinned by bioinformatic and empirical data. However, interactome data have not been produced. Conserved protein-protein interactions in other organisms, termed interologs, can be used to transfer interactions between species, allowing systems-level analysis in non-model organisms. RESULTS: Here, we describe a probabilistic, integrated network of interologs for the H. microstoma proteome, based on conserved protein interactions found in eukaryote model species. Almost a third of the 10,139 gene models in the v.3 assembly could be assigned interaction data and assessment of the resulting network indicates that topologically-important proteins are related to essential cellular pathways, and that the network clusters into biologically meaningful components. Moreover, network parameters are similar to those of single-species interaction networks that we constructed in the same way for S. cerevisiae, C. elegans and H. sapiens, demonstrating that information-rich, system-level analyses can be conducted even on species separated by a large phylogenetic distance from the major model organisms from which most protein interaction evidence is based. Using the interolog network, we then focused on sub-networks of interactions assigned to discrete suites of genes of interest, including signalling components and transcription factors, germline multipotency genes, and genes differentially-expressed between larval and adult worms. Results show not only an expected bias toward highly-conserved proteins, such as components of intracellular signal transduction, but in some cases predicted interactions with transcription factors that aid in identifying their target genes. CONCLUSIONS: With key helminth genomes now complete, systems-level analyses can provide an important predictive framework to guide basic and applied research on helminths and will become increasingly informative as new protein-protein interaction data accumulate.

Molecular data confirm the taxonomic position of Hymenolepis erinacei (Cyclophyllidea: Hymenolepididae) and host switching, with notes on cestodes of Palaearctic hedgehogs (Erinaceidae).

The cestode Hymenolepis erinacei is regarded as a widely distributed parasite in European hedgehogs of the genus Erinaceus, although the taxonomic position of this hymenolepidid has been debated for a considerable period of time. We present the first molecular data for this cestode, including partial DNA sequences of mitochondrial 16S and nuclear 28S ribosomal genes. Molecular phylogenetic analysis clusters H. erinacei in one clade together with representatives of the genus Hymenolepis from rodents. Characteristic morphological features, including the oval embryophore without filaments and shape of the embryonic hooks of H. erinacei are described. Features of these cestode eggs are proposed as a basis for non-invasive detection of parasitic infections in small mammal populations. The present study explores phylogenetic relationships within the genus Hymenolepis and the host switching related to H. erinacei. Cases of host switching in other genera of the family Hymenolepididae are reviewed. A short critical review of cestodes parasitizing hedgehogs in the Palaearctic is presented.

Survey of Hymenolepis spp. in pet rodents in Italy.

We carried out the first survey of Hymenolepis spp. infection in pet rodents in Italy. Fresh fecal samples were collected from 172 pet rodents as follows: guinea pigs (Cavia porcellus; n = 60), squirrels (Callosciurus finlaysonii, Callosciurus prevosti, Tamias striatus, Tamias sibiricus, Sciurus calorinensis; n = 52), hamsters (Phodopus campbelli, Mesocricetus auratus; n = 30), chinchillas (Chinchilla lanigera; n = 13), rats (Rattus norvegicus; n = 10), and mice (Mus minutoides; n = 7). These animals were housed either in pet shops or in private houses. All fecal samples were processed using the FLOTAC pellet technique to assess the number of eggs per gram (EPG) of feces. Eggs of Hymenolepis nana were found in 24 out of 172 (13.9 %; 95 % confidence interval = 9.3-20.2 %) pet rodents. Of those rodents, 41.6 % (10/24) were rats (mean EPG = 55.7; range = 2-200), 29.2 % (7/24) mice (mean EPG = 64.5; range = 32-120), 25.0 % (6/24) were chinchillas (mean EPG = 25.5; range = 10-50), and 4.2 % (1/24) hamsters (P. campbelli) (EPG = 86.0). In addition, Hymenolepis diminuta eggs were found in 2 out of 172 (1.2 %; 95 % confidence interval = 0.2-4.6 %) rodents examined, both of which (100 %; 2/2) were pet squirrels (C. prevosti) (mean EPG = 10; range = 4-16). To the authors' knowledge, this is the first report of a natural infection of H. diminuta in pet squirrels.

Description of two new species of Hymenolepis Weinland, 1858 (Cestoda: Hymenolepididae) from rodents on Luzon Island, Philippines.

Our helminthological examination of murid rodents on Luzon Island, Philippines, revealed a remarkable diversity of Hymenolepis Weinland, 1858. Here we describe two new species based on specimens from murid rodents Rattus everetti (Günther) and Apomys datae (Meyer) collected from Luzon Island. Hymenolepis alterna n. sp. differs from all known species of Hymenolepis in having irregularly alternating genital pores. This feature has not been reported from any previously known member of Hymenolepis. Additionally, Hymenolepis alterna n. sp. also differs from other Hymenolepis spp. in the relative position of both poral and antiporal dorsal osmoregulatory canals which are shifted towards the middle of the proglottis in relation to the ventral canals on both sides of the proglottides, and in having curved or twisted external seminal vesicle, covered externally by a dense layer of intensely stained cells. Hymenolepis bilaterala n. sp. differs from all known species of Hymenolepis in the relative position of both poral and antiporal dorsal osmoregulatory canals, which are shifted bilaterally towards the margins of proglottides in relation to the ventral canals, and in possession of testes situated in a triangle and eggs with very thin outer coat. A total of seven species of Hymenolepis are known from the Philippine archipelago. This total includes the cosmopolitan species Hymenolepis diminuta (Rudolphi, 1819), which was likely introduced to the island with invasive rats. Strikingly, all seven known species occur on the island of Luzon alone. By comparison, only six Hymenolepis spp. are known from the whole Palaearctic and seven from the Nearctic despite a much better level of knowledge of rodent helminths in these zoogeographical regions, as well as vast territories, diverse landscapes and very rich rodent fauna. This suggests that Hymenolepis spp. may have undergone an unusually active radiation in the Philippines. Possible explanations of this phenomenon are discussed.

Mebendazole in the treatment of Hymenolepis nana infections in the captive ring-tailed lemur (Lemur catta), China.

The present study was conducted to evaluate the effectiveness of mebendazole in the treatment of Hymenolepis nana infection in ring-tailed lemurs (Lemur catta). Ten (L. catta) from the Chengdu Zoological Garden in China, which were naturally infected with H. nana, were treated with mebendazole (10 mg/kg for 5 days). A posttreatment fecal examination was conducted 10 and 20 days after the start of treatment. All treatments resulted in a decrease in the number of eggs per gram in the posttreatment sample compared with the pretreatment sample. Reduction of mean egg count was 97.6% and 100% on days 10 and 20, respectively. The results indicated that mebendazole has marked efficacy against H. nana infections in L. catta.

Morphological features of Cloacotaenia megalops (Nitzsch in Creplin, 1829) (Cestoda, Hymenolepididae) from different hosts.

The tapeworm species Cloacotaenia megalops (Nitzsch in Creplin, 1829) is characterized by a very specific morphology. A particularly distinct feature is a large almost square scolex in which four fleshy suction cups are embedded and a rudimentary rostellum. During standard studies of wild duck cestode fauna in northwestern Poland, some morphological differences were observed among specimens, mainly in the shape of scolices and hermaphroditic proglottids of C. megalops isolated from different bird species. This paper attempts to demonstrate the impact of the host species on morphology of the parasite. The study material consisted of 39 individuals of C. megalops (19 from Aythya fuligula, 10 from Anas platyrhynchos, 4 from Bucephala clangula, 4 from Aythya marila and 2 from A. ferina). The isolated parasites were fixed and stored in 70% ethanol and solid preparations were made. Selected external and internal structures of the parasite were measured and photographed using a Zeiss microscope, a microscope camera Opta Tech 2.1 and Opta View 6.0.2.2. It was stated that the sizes of the most important elements of the parasite morphology are generally consistent with those presented in the available literature, nevertheless some differences were observed in both morphology and sizes of some anatomical structures, especially in the form of scolices and hermaphroditic proglottids between specimens isolated from hosts representing three different eco-tribes (Aythyini, Anatini and Mergini).

[On the species independence of Mathevolepis larbicus Karpenko, 1982 (Cyclophyllidea, Hymenolepididae, Ditestolepidini)].

The cestode species Mathevolepis larbicus Karpenko, 1982 parasitizing shrews in Russian Far East is restored. As the holotype was lost, the neotype is selected. The redescription and differential diagnosis of the species are given.

Pseudanoplocephala crawfordi is a member of genus Hymenolepis based on phylogenetic analysis using ribosomal and mitochondrial DNA sequences.

Pseudanoplocephala crawfordi is one of the important zoonotic cestodes causing economic significance and public health concern. In the present study, the phylogenetic position of P. crawfordi isolated from pigs was re-inferred using molecular markers of internal transcribed spacer ribosomal DNA (ITS rDNA) and partial NADH dehydrogenase subunit 1 (pnad1) mitochondrial DNA. The lengths of ITS1, ITS2 rDNA and pnad1 were 757 bp, 628 bp and 458 bp, respectively. Sequence differences in the ITS1, ITS2 rDNA and pnad1 between P. crawfordi and Hymenolepis species were smaller than that between cestodes within genus Hymenolepis. Phylogenetic analyses based on three gene fragments showed that P. crawfordi was grouped into cluster of Hymenolepis species. These results suggested that P. crawfordi would be one member of genus Hymenolepis but not in a new genus Pseudanoplocephala.

Cryptic diversity in hymenolepidid tapeworms infecting humans.

An adult hymenolepidid tapeworm was recovered from a 52-year-old Tibetan woman during a routine epidemiological survey for human taeniasis/cysticercosis in Sichuan, China. Phylogenetic analyses based on sequences of nuclear 28S ribosomal DNA and mitochondrial cytochrome c oxidase subunit 1 showed that the human isolate is distinct from Hymenolepis diminuta and Hymenolepis nana, the common parasites causing human hymenolepiasis. Proglottids of the human isolate were unfortunately unsuitable for morphological identification. However, the resultant phylogeny demonstrated the human isolate to be a sister species to Hymenolepis hibernia from Apodemus mice in Eurasia. The present data clearly indicate that hymenolepidid tapeworms causing human infections are not restricted to only H. diminuta and H. nana.

Detection of the rodent tapeworm Rodentolepis (=Hymenolepis) microstoma in humans. A new zoonosis?

A longitudinal survey of gastro-intestinal parasites was conducted over a 3-year period in remote communities in the north-west of Western Australia where, based on diagnosis by microscopy of faecal samples, Rodentolepis (=Hymenolepis) nana was found to be the most common enteric parasite. In the present study, using molecular tools, we describe the unexpected discovery, of a mixed infection with a second hymenolepidid species, Rodentolepis (=Hymenolepis) microstoma in four of the surveyed individuals. In the absence of any reliable earlier reports we believe this is to be the first instance of the detection of R. microstoma from human hosts. The development of a diagnostic restriction fragment polymorphism has enabled the study of R. microstoma in human populations and will greatly facilitate a more thorough understanding of the epidemiology of this parasite in the future.

Variation in the sizes of eggs and oncospheres and the numbers and distributions of testes in the tapeworm, Hymenolepis diminuta.

Four "strains" of Hymenolepis diminuta were examined for morphological variation. These included the ARME "strain" (currently maintained at the University of Keele, U.K.), the OSU "strain" (currently maintained at The Ohio State University) and the TOR (or UT) "strain" (currently maintained at the University of Toronto), all of which were derived from the parental RICE "strain," and the ANU "strain" (currently maintained at the Australian National University). Additionally, 2 separate "clonal" populations (populations derived from single cysticercoids) from both the OSU and ANU "strains" were examined. All "strains" and "clones" were maintained under identical conditions using Tenebrio molitor and male Sprague-Dawley rats as the intermediate and definitive hosts, respectively. The lengths and widths of eggs and larvae (oncospheres) passed in the hosts' feces, and the numbers and distributions of testes in proglottids were quantified and the data analyzed. Although analyses of the lengths and widths of eggs and larvae demonstrated significant differences among some "strains" and "clones," a discriminate analysis of the data indicated these parameters to be of questionable taxonomic significance. The eggs of all "strains" and "clones" consisted of 2 distinct populations differing in density and size but not infectivity; the relative proportions of eggs in the 2 populations were not determined. Considering all possible numbers and distributions of testes, 17 variations were seen in the strobilae of tapeworms. Analyses of the data demonstrated that the "strains" and "clones" could be differentiated clearly using only the frequencies of the 1p2a (1 poral and 2 aporal testes) or 1p3a distribution, or the frequencies of proglottids containing 3 or 4 testes; all other variations failed to clearly differentiate or group the various "strains" and "clones."(ABSTRACT TRUNCATED AT 250 WORDS)

A new species of Mathevotaenia (Cestoda: Anoplocephalidae) and other tapeworms from marsupials in Argentina.

Cestodes are reported from Didelphis albiventris Lund, 1840 and Micoureus cinereus Temminck, 1824 (Marsupialia: Didelphidae) in Argentina. These include a new species of Mathevotaenia Akhumyan, 1946 (Cestoda: Anoplocephalata) as well as M. bivittata (Janicki, 1904) and an unknown hymenolepidid cestode. Mathevotaenia argentinensis n. sp. is characterized by a relatively narrow strobila, 18-37 mm in total length and 1.0-1.5 mm in maximum width, 135-163 craspedote proglottids, 19-27 testes, and a muscular genital atrium. This species differs from M. didelphidis (Rudolphi, 1819) in the disposition of the genital ducts between the excretory canals and in the entrance of the vagina into the genital atrium posterior to the cirrus pouch; from M. paraguayae Schmidt and Martin, 1978 in the disposition of the genital ducts, absence of a seminal receptacle, and presence of an armed cirrus; and from M. boliviana Sawada and Harada, 1986 and M. pennsylvanica Chandler and Melvin, 1951 in the presence of an armed cirrus. Linstowiines appear to be the dominant cestodes in New World marsupials, with M. bivittata representing the most prevalent and widely distributed species. The hymenolepidid is the first record of this family in Neotropical marsupials.

Specific cross-immunity between Hymenolepis nana and H. diminuta: effects of transfer of immunity with homologous and heterologous immune mesenteric lymph node cells in BALB/c mice.

In BALB/c mice, Hymenolepis nana and H. diminuta stimulate a strong response. Accelerated expulsion of adult worms, as well as protection against larvae, occurred anamnestically when homologous or heterologous mesenteric lymph node cells from immune mice were transferred before challenge. The results further support the hypothesis that worm expulsion is a thymus dependent phenomenon. The extensive cross reactivity found is discussed in relation to the distinctive characteristics of the two worms. These results strongly suggest that there are antigenic similarities between the two parasites and that the accelerated expulsion of heterologous challenge infections is the result of a specific response to shared antigens.

Immunity to adult cestodes: basic knowledge and vaccination problems. A review.

Immunity in mammals to intestinal cestodes has been reviewed using the normal final host infected with the tapeworms Hymenolepis diminuta in rats and H. microstoma and H. nana in mice as a model. Primary infections up to a certain level continue to live as long the host, while most worms in infections with larger doses are destrobilated and expelled. It has been argued that concomitant immunity against a superimposed infection exists in rats and mice infected with H. diminuta and H. microstoma, respectively, and suggested that it also takes place in humans infected with Taenia spp. Immunity to secondary infections after expulsion of a primary infection occurs, but immunological memory is rather short-lived, although depression of worm growth occurs for at least two third of the rat's life. Serum antibodies have been shown to produce a direct precipitate on the surface of cestodes in vitro, but a direct effect of antibodies in vivo or the relationship with e.g. host effector cells, like mast cells and eosinophils, is unknown. It has been shown that peritoneal exudate cells from rats are able to kill H. diminuta in vitro. Very little is known about the mechanisms of tapeworms to counteract host immunological responses, but the tegumental glycoconjugates and discoidal secretory bodies are possible candidates. Passive transfer of immunity by mesenteric lymph node cells has only been successful using cells from H. nana egg-infected mice and has shown that only short-lived proliferating cells are responsible for transferring immunity. Vaccination procedures and problems are discussed with special reference to E. granulosus in dogs.

Digeneans and cestodes parasitic in the white-faced ibis Plegadis chihi (Aves: Threskiornithidae) from Argentina.

Some digeneans and cestodes parasitic in a population of the white-faced ibis Plegadis chihi (Vieillot) from Buenos Aires province, Argentina, are presented. The digeneans Dietziella egregia (Dietz, 1909), Patagifer bilobus (Rudolphi, 1819), Ascocotyle (Leighia) hadra Ostrowski de Nuñez, 1992 and Posthodiplostomum nanum Dubois, 1937 from the intestine; Prosthogonimus ovatus (Rudolphi, 1803) from the cloaca; Athesmia heterolecithodes (Braun, 1899) from the bile ducts and the cestode Hymenolepis megalops (Nitzsch in Creplin, 1829) from the cloaca, were recorded. The discovery of D. egregia, P. ovatus, A. heterolecithodes and P. nanum constitute new host and/or new geographical records. Adults of A. (L.) hadra, previously described in experimental definitive hosts, are first reported from a naturally infected bird. Hymenolepis megalops, a cestode of Anseriformes is first reported from Ciconiiformes.

[Classification of Hymenolepis macrorchida in the genus Idiogenoides (Cestoda, Davaineidae)]. / O prinadlezhnosti Hymenolepis macrorchida k rodu Idiogenoides (Cestoda, Davaineidae).

Hymenolepis macrorchida (Kotlan, 1921), a cestode of New Guinea parrots, possessing a small number (3 to 4) of testicles, belonging to the family Hymenolepididae to which it has been assigned for more than half of the century, is transferred to the family Davaineidae and designated as Idiogenoides macrorchida (Kotlan, 1921) comb. n.

[The systematic position of Hymenolepididae (Cestoda) from Australian marsupials]. / O sistematicheskom polozhenii gimenolepidid (Cestoda) iz avstraliiskikh sumchatykh.

A review of Hymenolepididae from Australian Marsupialia is given. These cestodes are transmitted out of the genus Hymenolepis, into which they were previously included. 3 species of them are transmitted to the genus Rodentolepis, and 7 species are arranged as a new genus Potorolepis. The diagnosis of Potorolepis and a list of species included are given. Possible phylogenetic relations of the genus Potorolepis with nearest groups of cestodes are discussed.

[Life cycles of the Hymenolepis, Aploparaksis birulai Linstow, 1905 and Aploparaksis brachyphallos (Krabbe, 1869)]. / Zhiznennye tsikly Tsestod - Gimenolepidid Aploparaksis birulai Linstow, 1905 i Aploparaksis brachyphallos (Krabbe, 1869)

Larvae of A. birulai from Lumbriculus variegatus and A. brachyphallos from Stylodrilus sp. from the Chauna lowland (Chukotka) are described. The species belonging of the larvae was proved experimentally. It was shown that Cysticercus sp. Hrabe, 1958 is a larvacyst of A. birulai. For larvacysts of A. birulai type the name of "floricerk" was suggested and for those of A. brachyphallos type--the name "tailed diplocyst". It is noted that A. uelcal Spassky et Jurpalova, 1968 is a synonym of A. brachyphallos (Krabbe, 1869) nec A. brachyphallos sensu Davies, 1938.

[Comparison of the variability of tapeworms obtained as a result of infecting rats with Hymenolepis diminuta larvae of different ages]. / Porównanie zmiennosci tasiemców uzyskanych w wyniku zarazenia szczurów larwami Hymenolepis diminuta w róznym wieku.

In Hymenolepis diminuta WMS "strain" tapeworms which were obtained 2.5 months after the administration to rats of 2-month old larvae--cysticercoids++, isolated from Tribolium destructor, only one-sided position of genital pores (PGP) developed. The extended 7-month duration of the invasion of H. diminuta larvae stimulates the development of variable PGP already in 14.1% of 2.5-month tapeworms. In tapeworms with exclusively one-sided PGP in the first of the two groups mentioned, the number of type 1p2a proglottids (1 testis on the poral side and 2 testes on the aporal side) as well as type 0p3a, 1p3a and 2p1a amounted to 88.2%, 5.5%, 4.2% and 0.5%, respectively and similarly in the second group--88.3%, 5.6%, 4.5% and 0.6%, respectively. In tapeworms with variable PGP the mean number of the types of proglottids mentioned was different from (86.0%, 4.1%, 3.8% and 4.1%, respectively) the same figure in tapeworms with one-sided PGP. Particularly high correlation was found to occur between the number of PGP variations and type 2p1a proglottids (r = +0.928, P < 0.01).

[Revision of Aploparaksis crassirostris and A. sinensis (Cestoda: Hymenolepididae)]. / Reviziia vidov Aploparaksis crassirostris i A. sinensis (Cestoda: Hymenolepididae).

Based on the examination of specimens of Apoloparaksis crassirostris deposited in the Museum of Zoology in Copenhagen and the Museum of Natural History in Geneva and cestode material from other collections, we have carried out the revision of this species, designated the lectotype and paralectotypes, made its redescriptions, enumerated synonyms, showed the only host of this species in the snipe Gallinago gallinago, and more precisely mapped the distribution range of the parasite. The investigation of the type series of A. sinensis, the parasite of the woodcock Scolopax rusticola, deposited in the Museum of Natural History in Geneva, confirmed the validity of this species, earlier considered as synonym of A. crassirostris. The lectotype and paralectotypes of A. sinensis were designated. Some data on its life cycle have been obtained. It was also found by the experimental invasion that five species of oligochaetes of the family Lumbricidae are intermediate hosts. The metacestodes of this species belongs to the tailed diplocyst modification and posesses a characteristic feature, the bifurcation of tail.