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Parasites, Clonorchis Sinensis and Opisthorchis Viverrini

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Parasites, Clonorchis Sinensis and Opisthorchis Viverrini Unlocking the Transcriptomes of Two Carcinogenic Parasites, Clonorchis sinensis and Opisthorchis viverrini Neil D. Young1*, Bronwyn E. Campbell1, Ross S. Hall1, Aaron R. Jex1, Cinzia Cantacessi1, Thewarach Laha2, Woon-Mok Sohn3, Banchob Sripa4, Alex Loukas5, Paul J. Brindley6, Robin B. Gasser1* 1 Department of Veterinary Science, The University of Melbourne, Werribee, Victoria, Australia, 2 Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, 3 Department of Parasitology and Institute of Health Sciences, School of Medicine, Gyeongsang National University, Jinju, Republic of Korea, 4 Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, 5 Queensland Tropical Health Alliance, James Cook University, Smithfield, Cairns, Queensland, Australia, 6 Department of Microbiology, Immunology and Tropical Medicine, The George Washington University Medical Center, Washington, D. C., United States of America Abstract The two parasitic trematodes, Clonorchis sinensis and Opisthorchis viverrini, have a major impact on the health of tens of millions of humans throughout Asia. The greatest impact is through the malignant cancer ( = cholangiocarcinoma) that these parasites induce in chronically infected people. Therefore, both C. sinensis and O. viverrini have been classified by the World Health Organization (WHO) as Group 1 carcinogens. Despite their impact, little is known about these parasites and their interplay with the host at the molecular level. Recent advances in genomics and bioinformatics provide unique opportunities to gain improved insights into the biology of parasites as well as their relationships with their hosts at the molecular level. The present study elucidates the transcriptomes of C. sinensis and O. viverrini using a platform based on next-generation (high throughput) sequencing and advanced in silico analyses. From 500,000 sequences, .50,000 sequences were assembled for each species and categorized as biologically relevant based on homology searches, gene ontology and/or pathway mapping. The results of the present study could assist in defining molecules that are essential for the development, reproduction and survival of liver flukes and/or that are linked to the development of cholangiocarcinoma. This study also lays a foundation for future genomic and proteomic research of C. sinensis and O. viverrini and the cancers that they are known to induce, as well as novel intervention strategies. Citation: Young ND, Campbell BE, Hall RS, Jex AR, Cantacessi C, et al. (2010) Unlocking the Transcriptomes of Two Carcinogenic Parasites, Clonorchis sinensis and Opisthorchis viverrini. PLoS Negl Trop Dis 4(6): e719. doi:10.1371/journal.pntd.0000719 Editor: Malcolm K. Jones, University of Queensland, Australia Received February 18, 2010; Accepted April 28, 2010; Published June 22, 2010 Copyright: ß 2010 Young et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funding from the Australian Research Council is gratefully acknowledged (RBG). NDY was the grateful recipient of an Endeavour Award from the Australian Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (NDY); [email protected] (RBG) Introduction asexual reproduction takes place, and freshwater cyprinid fishes or palaemonid shrimps (for C. sinensis only) as intermediate hosts. Liver flukes (Platyhelminthes: Digenea) include important food- Fish–eating ( = piscivorous) mammals, including humans, dogs and borne eukaryotic pathogens of humans [1–5]. For example, the cats, act as definitive hosts, in which sexual reproduction occurs. liver flukes Clonorchis sinensis and Opisthorchis viverrini, which cause Clonorchiasis and opisthorchiasis are prevalent in geographical the diseases clonorchiasis and opisthorchiasis, respectively, repre- regions where raw cyprinid fish (C. sinensis and O. viverrini) and/or sent a substantial public health problem in many parts of Asia shrimp (C. sinensis) are a staple of the diet of humans [2,12]. Both [2,3,6]. Clonorchis sinensis is endemic predominantly in regions of parasites establish in the bile ducts of the liver as well as China (including Hong Kong and Taiwan), Korea and North extrahepatic ducts and the gall bladder of the mammalian Vietnam [2,6], whilst O. viverrini is endemic throughout Thailand, (definitive) host. These parasites are long-lived and cause chronic the Lao People’s Democratic Republic, Vietnam and Cambodia cholangitis, which can lead to periductal fibrosis, cholecystitis and [7]. Both of these parasites cause immense suffering in tens of cholelithiasis, obstructive jaundice, hepatomegaly and/or fibrosis millions of people, and more than 600 million people are of the periportal system [13–18]. Importantly, both experimental estimated to be at risk of infection [2,8]. Despite efforts to control and epidemiological evidence [19–22] strongly implicates C. these two liver flukes, the prevalence of infection can be as high as sinensis and O. viverrini infections in the etiology of cholangiocarci- 70% in some regions, including the Guangxi province in China (C. noma, a malignant cancer of the bile ducts in humans which has a sinensis) and Khon Kaen province in Thailand (O. viverrini) [2,7]. A very poor prognosis. Indeed, C. sinensis and O. viverrini are both related fluke, O. felineus, is endemic in Siberia and eastern regions categorized by the International Agency for Research on Cancer of the former USSR, and causes a similar disease and disease (IARC) as Group 1 carcinogens [23]. burden to O. viverrini and C. sinensis [4]. In humans, the onset of cholangiocarcinoma occurs with The life cycles of C. sinensis and O. viverrini are similar [9–11], chronic clonorchiasis or opisthorchiasis, associated with hepato- involving an aquatic snail (order Mesogastropoda), in which biliary damage, inflammation, periductal fibrosis and/or cellular www.plosntds.org 1 June 2010 | Volume 4 | Issue 6 | e719 The Transcriptomes of the Asian Liver Flukes Author Summary initiate and enhance the development of cholangiocarcinoma [29,34]. The parasitic worms, Clonorchis sinensis and Opisthorchis To date, most molecular biological research of socioeconomi- viverrini, have a serious impact on the health of tens of cally important trematodes has focused on the human blood millions of people throughout Asia. The greatest impact, flukes, Schistosoma mansoni and S. japonicum, recently culminating in however, is through the malignant, untreatable cancer the determination of their nuclear genome sequences [35,36]. (cholangiocarcinoma) that these parasites induce in These genomic data sets provide an invaluable resource to support chronically infected people. These liver flukes are officially the exploration of the fundamental biology and evolution of flukes classified by the World Health Organization (WHO) as as well as their host–parasite interactions [36]. However, the Group 1 carcinogens. In spite of their massive impact on biology of schistosomes, which live as dioecious adults in the blood human health, little is known about these parasites and stream of mammalian hosts, is vastly distinct from that of their relationship with the host at the molecular level. hermaphroditic liver flukes, such as C. sinensis and O. viverrini. Here, we provide the first detailed insight into the , transcriptomes of these flukes, providing a solid founda- Currently, a total of only 8,000 expressed sequence tags (ESTs) tion for all of the molecular/-omic work required to are publicly available for C. sinensis [37–39] and O. viverrini [40], a understand their biology, but, more importantly, to dataset far too small to give sufficient insights into transcriptomes elucidate key aspects of the induction of cholangiocarci- for the purpose of supporting genomic and other fundamental noma. Although our focus has been on the parasites, the molecular research. implications will extend far beyond the study of parasitic Some recent genomic, bioinformatic and proteomic studies disease. Importantly, insights into the pathogenesis of the [29,41–45] indicate unique and exciting prospects to explore key infection are likely to have major implications for the study biochemical, physiological and biological pathways in liver flukes, and understanding of other cancers. and to predict and prioritize novel drug targets. In particular, the characterization of the transcriptome of the common liver fluke, Fasciola hepatica using next-generation sequencing-bioinformatic responses to antigens from the infecting fluke [24]. These platform has discovered numerous molecules of biological conditions predispose to cholangiocarcinoma, possibly through relevance, some of which are inferred to be involved in key an enhanced susceptibility of DNA to damage by carcinogens biological processes or pathways that could serve as key targets for [19,20,25–27]. Chronic hepatobiliary damage is reported to be new trematocidal drugs or vaccines [46]. Using a similar platform, multi-factorial and considered to arise from a continued we characterized herein the transcriptomes of the adult stages of C. mechanical irritation of the epithelium by the flukes
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