Cestode genomics - progress and prospects for advancing basic and applied aspects of flatworm biology

Department of Zoology, The Natural History Museum, London, UK.
Parasite Immunology (Impact Factor: 2.14). 07/2012; 34(2-3):130-50. DOI: 10.1111/j.1365-3024.2011.01319.x
Source: PubMed


Characterization of the first tapeworm genome, Echinococcus multilocularis, is now nearly complete, and genome assemblies of E. granulosus, Taenia solium and Hymenolepis microstoma are in advanced draft versions. These initiatives herald the beginning of a genomic era in cestodology and underpin a diverse set of research agendas targeting both basic and applied aspects of tapeworm biology. We discuss the progress in the genomics of these species, provide insights into the presence and composition of immunologically relevant gene families, including the antigen B- and EG95/45W families, and discuss chemogenomic approaches toward the development of novel chemotherapeutics against cestode diseases. In addition, we discuss the evolution of tapeworm parasites and introduce the research programmes linked to genome initiatives that are aimed at understanding signalling systems involved in basic host-parasite interactions and morphogenesis.

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Available from: Klaus Brehm,
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    • "have contributed to some of the important differences in larval morphology and development found between these closely related species (Thompson 1986). These differences have long been considered puzzling, particularly since the gene complement of both species is almost identical and no notable differences in genome organization had been identified between them so far (Olson et al. 2012; Tsai et al. 2013). The genes showing transcriptional fusions to upstream solo-LTRs have a variety of roles in important biological pathways. "
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    ABSTRACT: Taeniid cestodes (including the human parasites Echinococcus spp. and Taenia solium) have very few mobile genetic elements (MGEs) in their genome, despite lacking a canonical PIWI pathway. The MGEs of these parasites are virtually unexplored, and nothing is known about their expression and silencing. In this work, we report the discovery of a novel family of small non-autonomous Long Terminal Repeat retrotransposons (also known as Terminal Repeat Retrotransposons in Miniature, TRIMs) which we have named ta-TRIM (taeniid TRIM). ta-TRIMs are only the second family of TRIM elements discovered in animals, and are likely the result of convergent reductive evolution in different taxonomic groups. These elements originated at the base of the taeniid tree and have expanded during taeniid diversification, including after the divergence of closely related species such as E. multilocularis and E. granulosus. They are massively expressed in larval stages, from a small proportion of full-length copies and from isolated terminal repeats that show transcriptional read-through into downstream regions, generating novel non-coding RNAs and transcriptional fusions to coding genes. In E. multilocularis, ta-TRIMs are specifically expressed in the germinative cells (the somatic stem cells) during asexual reproduction of metacestode larvae. This would provide a developmental mechanism for insertion of ta-TRIMs into cells that will eventually generate the adult germ line. Future studies of active and inactive ta-TRIM elements could give the first clues on MGE silencing mechanisms in cestodes. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Genome Biology and Evolution 07/2015; 7(8):2136. DOI:10.1093/gbe/evv126 · 4.23 Impact Factor
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    • "H. diminuta, like many parasites, has reduced its genome size (Olson et al., 2012; Tsai et al., 2013) and simplified its body plan while maximizing fitness in the host environment. Tapeworms have evolved unique structures and strategies that facilitate their parasitic needs. "
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    ABSTRACT: Tapeworms are pervasive and globally distributed parasites that infect millions of humans and livestock every year, and are the causative agents of two of the 17 neglected tropical diseases prioritized by the World Health Organization. Studies of tapeworm biology and pathology are often encumbered by the complex life cycles of disease-relevant tapeworm species, that infect hosts such as foxes, dogs, cattle, pigs, and humans. Thus, studies of laboratory models can help overcome the practical, ethical, and cost-related difficulties faced by tapeworm parasitologists. The rat intestinal tapeworm Hymenolepis diminuta is easily reared in the laboratory and has the potential to enable modern molecular-based experiments that will greatly contribute to our understanding of multiple aspects of tapeworm biology such as growth and reproduction. As part of our efforts to develop molecular tools for experiments on H. diminuta, we have characterized a battery of lectins, antibodies, and common stains that label different tapeworm tissues and organ structures. Using confocal microscopy, we have assembled an "atlas" of H. diminuta organ architecture that will be a useful resource for helminthologists. The methodologies we describe will facilitate characterization of loss-of-function perturbations using H. diminuta, in order to understand fundamental aspects of tapeworm biology that may aid efforts to discover new therapeutic targets to eradicate these parasites. Copyright © 2015 The Authors. Published by Elsevier Inc. All rights reserved.
    Experimental Parasitology 06/2015; DOI:10.1016/j.exppara.2015.05.015 · 1.64 Impact Factor
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    • "To date, discussions of the emergence of platyhelminth parasitism have focused on organismic and morphological traits—in other words, those character systems for which data have been historically available. However, principally because of their importance as human pathogens, genomic data are now available from all major lineages of Neodermata, including well-curated assemblies, annotation efforts, and experimental protocols for species such as Echinococcus multilocularis (Brehm, 2010; Olson et al., 2012; Tsai et al., 2013) and Schistosoma mansoni (Collins et al., 2013; Wang et al., 2013). With such data available, there has been much discussion of the genome-level adaptations to parasitism, with suggestions of many apparent losses, including several homeobox genes, vasa, tudor, and piwi orthologs, fatty and amino acid biosynthesis pathways, and peroxisome components; proposed gains include the evolution of a neodermatan-specific Argonaute subfamily and micro-exon gene organization (Tsai et al., 2013; Hahn et al., 2014). "
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    ABSTRACT: Flatworms number among the most diverse invertebrate phyla, and represent the most biomedically significant branch of the major bilaterian clade Spiralia, but to date, deep evolutionary relationships within this group have been studied using only a single locus (the rRNA operon), leaving the origins of many key clades unclear. Here, using a survey of genomes and transcriptomes representing all free-living flatworm orders, we provide resolution of platyhelminth interrelationships based on hundreds of nuclear protein-coding genes, exploring phylogenetic signal through concatenation as well as recently developed consensus approaches. These analyses robustly support a modern hypothesis of flatworm phylogeny, one which emphasizes the primacy of the often-overlooked 'microturbellarian' groups in understanding the major evolutionary transitions within Platyhelminthes: perhaps most notably, we propose a novel scenario for the interrelationships between free-living and vertebrate-parasitic flatworms, providing new opportunities to shed light on the origins and biological consequences of parasitism in these iconic invertebrates.
    eLife Sciences 03/2015; 4. DOI:10.7554/eLife.05503 · 9.32 Impact Factor
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