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.

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.

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.

Two new species of Hymenolepis (Cestoda: Hymenolepididae) from murid rodents (Rodentia: Muridae) in the Philippines.

Two previously unrecognized species of the genus Hymenolepis are described based on specimens obtained from murid rodent species Bullimus luzonicus , Apomys microdon , and Rattus everetti collected on Luzon Island, Philippines. Hymenolepis bicauda n. sp. differs from all known Hymenolepis spp. in relative position of the poral dorsal and ventral osmoregulatory canals, gravid uterus occupying less than half the length of proglottid, relatively few eggs, and the highly characteristic longitudinal split of proglottids at the end of the gravid strobila. Hymenolepis haukisalmii n. sp. differs from all known Hymenolepis spp. in the relative position of both poral and aporal dorsal and ventral osmoregulatory canals and uterus lacking dorsal and ventral diverticula. The shift in the relative position of the dorsal and ventral osmoregulatory canals was not known in Hymenolepis from rodents in other regions of the world and is reminiscent of the situation observed in Hymenolepis erinacei, parasitic in hedgehogs, and members of the genus Talpolepis, parasitic in moles. The cosmopolitan species Hymenolepis diminuta was the only member of the genus previously reported from the Philippines.

Two new species of Hymenolepis (Cestoda: Hymenolepididae) from Spalacidae and Muridae (Rodentia) from eastern Palearctic.

Previously unrecognized species of the genus Hymenolepis are described based on specimens from spalacid and murid (Murinae) rodents. Hymenolepis rymzhanovi sp. nov. from the Siberian zokor, Myospalax myospalax (Laxmann), from East Kazakhstan, and H. apodemi sp. nov. from Eurasian field mice, Apodemus peninsulae (Thomas), A. uralensis (Pallas) and A. agrarius (Pallas), from the south of Russian Far East, western Siberia and south-eastern Kazakhstan are characterized. The new species differ from other species of the genus by the morphology of the scolex, the relative position and length of the cirrus-sac and the relative position and arrangement of the testes. Differential criteria of species of Hymenolepis (sensu stricto) are also discussed.

In vivo efficacy of the anthelmintic tribendimidine against the cestode Hymenolepis microstoma in a controlled laboratory trial.

Tribendimidine has been registered for the treatment of human soil transmitted helminthiases in China. In the model nematode Caenorhabditis elegans it is an agonist of L-subtype nicotinic acetylcholine receptors and therefore shares its mode of action with levamisole and pyrantel. Besides its broad spectrum of nematicidal efficacy, tribendimidine is efficacious against several trematodes and has been attributed to have anti-cestodal effects. However, there are few published data available for the latter. The efficacy of tribendimidine and its nematicidal metabolite deacylated amidantel against Hymenolepis microstoma were examined for their anti-cestodal potential. Doses of 50 and 100mg/kg body weight deacylated amidantel and 10, 25, 50, and 100mg/kg tribendimidine were administered orally on three consecutive days to mice experimentally infected with eight cysticercoids. Necropsy was performed and the worm burdens were determined one day after the last treatment. Furthermore, levamisole was used in combination with tribendimidine (100mg/kg levamisole plus 10 and 25mg/kg tribendimidine, respectively) and alone (50 and 100mg/kg) to investigate any possible interactions of the partner compounds against cestodes. Tribendimidine showed a very high efficacy at dosages of 50mg/kg or higher. Surprisingly, deacylated amidantel led to no reduction of the worm burden in any of the treatments. Combinations of levamisole with tribendimidine did not augment the effects of tribendimidine alone and as expected levamisole alone also showed no anti-cestodal activity. To our knowledge, this study shows for the first time activity of tribendimidine against a cestode in a controlled laboratory study. Due to the excellent cure rates observed here, multiple tribendimidine treatments might be considered as useful scheme for treatments of cestode, nematode and trematode infections although this would significantly increase both costs and management efforts. Moreover, the differences between tribendimidine and deacylated amidantel indicate at least a strong difference in sensitivity of H. microstoma or a strong difference in drug availability.

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.

Tapeworms of rock dove and domestic chicken in Taif area, Saudi Arabia.

The present study aimed to identify the tapeworms that parasitize the rock dove Columba livia palastinae and domestic chicken Gallus gallus domesticus in Taif governorate, Saudi Arabia. A total of 115 rock doves and 105 domestic chicken have been examined. Birds were brought in from the wells and farms inside and outside the city of Taif. In rock doves, the percentage of infection was recorded as Cotugnia digonopora 5.21%, Hymenolepis carioca 10.43%, Raillietina echinobothrida 27.82%, Raillietina tetragona 22.6%. The prevalence of infection recorded in Municipal chicken with different types of tapeworms was Cotugnia digonopora 7.61%, Choanotaenia infundibulum 12.38%, Amoebotaenia sphenoides 7.61%, Raillietina echinobothrida 11.42%, Raillietina tetragona 8.57%, Raillietina (Paroniella) kashiwarensis 4.76%. The overall percentage of infected rock pigeons Columba livia palastinae with tapeworms was 66.1% while the percentage of infected chicken Gallus gallus domestica was 52.3%. The study defined and described this species as classification keys in place.

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.

Helminth infections in small mammals from Ulu Gombak Forest Reserve and the risk to human health.

A survey for small mammal parasites carried out in a secondary forest of Ulu Gombak, Selangor, Peninsula Malaysia yielded the following animals: Rattus bowersi (7), Rattus tiomanicus jalorensis (2), Maxomys rajah (12), Maxoyms whiteheadi (3), Leopoldamys sabanus(13), Sundamys muelleri(10), Lariscus insignis (1), Sundasciurus tenuis (1) and Tupaia glis (2). The following nematodes: Capillaria hepatica, Hepatojarakus malayae, Trichostrongylus sp. and Streptopharagus sp., the following cestodes: Hymenolepis sp., Raillietina sp. and Taenia taeniaformis; and trematode, Zonorchis sp. from Tupaia glis were recovered. No parasites were observed during blood examination. No endoparasite was seen in Maxomys whiteheadi, Lariscus insignis and Sundasciurus tenuis. The following parasites, Capillaria hepatica, Hymenolepis sp., Raillietina sp. and Taenia taeniaformis are considered of medical importance.

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.

Hymenolepis pseudodiminuta Tenora et al. 1994 from Apodemus speciosus and H. diminuta: a comparison of experimental infections in rats.

The successful maintenance of Hymenolepis pseudodiminuta, isolated from Apodemus speciosus, is described for the first time. In the laboratory, the flour beetle, Tribolium confusum, and F344 rats could serve as intermediate and definitive hosts, respectively. In single worm infections with H. pseudodiminuta, which were carried in two groups of rats, adult worms were recovered from eight and seven out of ten rats, respectively, while Hymenolepis diminuta was found in all of ten rats 6 weeks after inoculation. The worm weight of H. pseudodiminuta in rats was significantly lower than that of H. diminuta. The egg output of H. pseudodiminuta occurred significantly earlier than that of H. diminuta. The number of eggs in the faeces of H. diminuta-infected rats was approximately twofold higher than the number in the faeces of H. pseudodiminuta-infected rats throughout the course of the infection. Mucosal mast cells in rats infected with H. pseudodiminuta were significantly more common than in rats infected with H. diminuta. No detectable IgE antibodies were found in the uninfected and H. diminuta-infected rat groups; however total IgE was detected in H. pseudodiminuta-infected rats but the concentrations were variable between individuals.

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.

[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.

A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species.

Since isolates of Hymenolepis nana infecting humans and rodents are morphologically indistinguishable, the only way they can be reliably identified is by comparing the parasite in each host using molecular tools. In the current study, isolates of H. nana from rodent and human hosts from a broad geographical range were sequenced at the ribosomal first internal transcribed spacer (ITS1), the mitochondrial cytochrome c oxidase subunit 1 (C01) gene and the nuclear paramyosin gene loci. Twenty-three isolates of H. nana were sequenced at the ITS1 locus and this confirmed the existence of spacers which, although similar in length (approximately 646 bp), differed in their primary sequences which led to the separation of the isolates into 2 clusters when analysed phylogenetically. This sequence variation was not, however, related to the host of origin of the isolate, thus was not a marker of genetic distinction between H. nana from rodents and humans. Sequencing of a 444 bp fragment of the mitochondrial cytochrome c oxidase 1 gene (C01) in 9 isolates of H. nana from rodents and 6 from humans identified a phylogenetically supported genetic divergence of approximately 5% between some mouse and human isolates. This suggests that H. nana is a species complex, or 'cryptic' species (=morphologically identical yet genetically distinct). A small segment of the nuclear gene, paramyosin, (625 bp or 840 bp) was sequenced in 4 mouse and 3 human isolates of H. nana. However, this gene did not provide the level of heterogeneity required to distinguish between isolates from rodent and human hosts. From the results obtained from faster evolving genes, and the epidemiological evidence, we believe that the life-cycle of H. nana that exists in the north-west of Western Australia is likely to involve mainly 'human to human' transmission.

Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that Platyhelminths are Eutrochozoans.

Using "long-PCR," we amplified in overlapping fragments the complete mitochondrial genome of the tapeworm Hymenolepis diminuta (Platyhelminthes: Cestoda) and determined its 13,900-nt sequence. The gene content is the same as that typically found for animal mitochondrial DNA (mtDNA) except that atp8 appears to be lacking, a condition found previously for several other animals. Despite the small size of this mtDNA, there are two large noncoding regions, one of which contains 13 repeats of a 31-nt sequence and a potential stem-loop structure of 25 bp with an 11-member loop. Large potential secondary structures were identified also for the noncoding regions of two other cestode mtDNAS: Comparison of the mitochondrial gene arrangement of H. diminuta with those previously published supports a phylogenetic position of flatworms as members of the Eutrochozoa, rather than placing them basal to either a clade of protostomes or a clade of coelomates.