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Clonorchis Sinensis Suggests Functions Beyond Sterol Binding and Transport Marziyeh Anari†, Andreas J

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Clonorchis Sinensis Suggests Functions Beyond Sterol Binding and Transport Marziyeh Anari†, Andreas J Anari et al. Parasites Vectors (2020) 13:38 https://doi.org/10.1186/s13071-020-3910-0 Parasites & Vectors RESEARCH Open Access Expanded complement of Niemann-Pick type C2-like protein genes in Clonorchis sinensis suggests functions beyond sterol binding and transport Marziyeh Anari†, Andreas J. Stroehlein†, Ross S. Hall, Bill C. H. Chang, Robin B. Gasser* and Neil D. Young* Abstract Background: The parasitic fatworm Clonorchis sinensis inhabits the biliary tree of humans and other piscivorous mammals. This parasite can survive and thrive in the bile duct, despite exposure to bile constituents and host immune attack. Although the precise biological mechanisms underlying this adaptation are unknown, previous work indicated that Niemann-pick type C2 (NPC2)-like sterol-binding proteins might be integral in the host-parasite interplay. Expan- sions of this family in some invertebrates, such as arthropods, have shown functional diversifcation, including novel forms of chemoreception. Thus, here we curated the NPC2-like protein gene complement in C. sinensis, and predicted their conserved and/or divergent functional roles. Methods: We used an established comparative genomic-bioinformatic approach to curate NPC2-like proteins encoded in published genomes of Korean and Chinese isolates of C. sinensis. Protein sequence and structural homol- ogy, presence of conserved domains and phylogeny were used to group and functionally classify NPC2-like proteins. Furthermore, transcription levels of NPC2-like protein-encoding genes were explored in diferent developmental stages and tissues. Results: Totals of 35 and 32 C. sinensis NPC2-like proteins were predicted to be encoded in the genomes of the Korean and Chinese isolates, respectively. Overall, these proteins had low sequence homology and high variability of sequence alignment coverage when compared with curated NPC2s. Most C. sinensis proteins were predicted to retain a conserved ML domain and a conserved fold conformation, with a large cavity within the protein. Only one protein sequence retained the conserved amino acid residues required in bovine NPC2 to bind cholesterol. Non-canonical C. sinensis NPC2-like protein-coding domains clustered into four distinct phylogenetic groups with members of a group frequently encoded on the same genome scafolds. Interestingly, NPC2-like protein-encoding genes were predicted to be variably transcribed in diferent developmental stages and adult tissues, with most being transcribed in the metacercarial stage. Conclusions: The results of the present investigation confrms an expansion of NPC2-like proteins in C. sinensis, sug- gesting a diverse array of functions beyond sterol binding and transport. Functional explorations of this protein family *Correspondence: [email protected]; [email protected] †Marziyeh Anari and Andreas J. Stroehlein contributed equally to this work Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC 3010, Australia © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Anari et al. Parasites Vectors (2020) 13:38 Page 2 of 10 should elucidate the mechanisms enabling the establishment and survival of C. sinensis and related fukes in the biliary systems of mammalian hosts. Keywords: Clonorchis sinensis, Comparative genomics, Niemann-pick type C2, NPC2, Functional protein annotation, Adaptation Background eukaryotes, NPC2 is encoded by a single copy gene. Parasitic fatworms (phylum Platyhelminthes; class In some mammals, this protein binds cholesterol and Trematoda) are responsible for neglected tropical dis- other lipids and transports them out of the lysosome to eases (NTDs) that afect more than 750 million humans other parts of the cell [19]. In arthropods, duplication and other mammals throughout the world, particularly and genetic diferentiation of NPC2 genes [20–23] have in Southeast Asia and the Western Pacifc regions [1–3]. led to new molecular functions, including chemorecep- Important trematode species include Clonorchis sin- tion via binding to semiochemical and other volatile ensis and Opisthorchis spp. [3, 4]. Te consumption of compounds [23–25]. Related proteins that contain a fsh containing the infective developmental stage (meta- conserved myeloid diferentiation factor-2 (MD-2)-re- cercaria) of these liver fukes leads to an infection that, lated lipid-binding (ML) domain are also reported to if chronic, can cause serious hepatobiliary diseases in play diverse roles in lipid metabolism, innate immunity humans, including clonorchiasis (C. sinensis) or opisthor- and/or chemoreception in arthropods [20, 26]. Despite chiasis (Opisthorchis spp.), particularly in Asia [3, 5–7]. the substantial expansion of the NPC2-like protein For example, C. sinensis impacts more than 35 million family in liver fukes, almost nothing is known, at the people across China, Japan, Korea and Vietnam [8, 9], molecular level, about their biological functions in such and has been classifed as a Class I carcinogen by the parasites and/or the regulation of host-pathogen inter- International Agency for Research on Cancer (IARC) actions. Here, we employed a bioinformatic workfow [10]. Despite the importance of this parasite, the molecu- to predict, curate and annotate NPC2-like proteins lar mechanisms that govern or modulate the interactions encoded in the draft genomes of a Korean and a Chi- between C. sinensis and its host animals remain largely nese isolate of C. sinensis. unknown. When piscivorous mammals (e.g. humans, dogs and Methods cats) consume fsh infected by C. sinensis, metacer- Inference of NPC2‑like protein sequences cariae excyst in the duodenum, and juveniles migrate Two C. sinensis genomes, one assembled from a Korean and develop to adult fukes in the biliary system [11, isolate (gene accession numbers beginning with “Cs- 12]. Te adult fukes can alter biliary duct pathology k2”; BioProject ID: PRJNA386618) [17] and one from via mechanical irritation and by releasing molecules to a Chinese isolate (gene accession numbers beginning facilitate feeding [13]. Furthermore, as the adult fukes with “csin”; BioProject ID: PRJNA72781) [18], and their grow and migrate, they can obstruct the bile duct and gene annotations were downloaded from the Worm- elevate bile duct pressure [6]. Clonorchiasis often leads Base ParaSite database (v.13; accessed 20 May 2019) to chronic hepatobiliary illness and can induce cholan- [27]. NPC2-like homologues in C. sinensis were initially giocarcinoma (CCA), a malignant cancer of the biliary identifed (Fig. 1, steps 1-3). First, homologues of nine system [1, 5, 14]. To better understand the pathogen- curated NPC2 proteins available in the SWISS-PROT esis of clonorchiasis and CCA, and to assist in eforts database (Table 1; accessed 20 May 2019) [28] were to control the parasite causing these diseases, research- identifed in the C. sinensis proteomes using BLASTp ers have explored the function of C. sinensis proteins, v.2.2.29 (E-value cut-of: 10) [29]. Second, a reciprocal including proteins likely to be important for establish- BLASTp (E-value cut-of: 10) search of homologues of ment and survival in the human biliary system. NPC2 proteins from SWISS-PROT against the NCBI In bile, cholesterol and phospholipids are abundant, non-redundant protein database (NCBI-nr; accessed and lipid-binding proteins (LBPs) have been proposed 20 May 2019) [30] was performed. Clonorchis sinensis to play an important role in maintaining the chemical NPC2-like protein homologues matching proteins sub- homeostasis of liver fukes in the bile duct [15]. Inter- mitted to NCBI-nr and annotated as “Niemann-pick estingly, gene duplication events have led to more than C2 protein”, “NPC intracellular cholesterol transport 20 copies of genes encoding homologues of a lipid- 2”, “Epididymal secretory protein E1” or “Epididy- binding protein, Niemann-Pick type C2 (NPC2), in the mal secretory protein E1-like”, or that lacked a protein genomes of C. sinensis and O. viverrini [16–18]. In most description (unnamed or hypothetical proteins), were Anari et al. Parasites Vectors (2020) 13:38 Page 3 of 10 retained. Tird, we searched for conserved domains in the predicted C. sinensis proteome using the program InterProScan v.5.15.54 [31], utilising the Pfam data- base v.27.0 [32]. Proteins with a conserved ML domain (Pfam identifer PF02221) were retained. Numbers of C. sinensis proteins with NPC2 homologues and/or a conserved ML
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