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Characterization of Trichuris Muris Secreted Proteins and Extracellular Vesicles Provides New Insights Into Host–Parasite Communication Ramon M

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Characterization of Trichuris Muris Secreted Proteins and Extracellular Vesicles Provides New Insights Into Host–Parasite Communication Ramon M JOURNAL OF EXTRACELLULAR VESICLES, 2018 VOL. 7, 1428004 https://doi.org/10.1080/20013078.2018.1428004 RESEARCH ARTICLE Characterization of Trichuris muris secreted proteins and extracellular vesicles provides new insights into host–parasite communication Ramon M. Eichenberger *a, Md Hasanuzzaman Talukder *b, Matthew A. Field a, Phurpa Wangchuk a, Paul Giacomina, Alex Loukas a and Javier Sotillo a aCentre for Biodiscovery and Molecular Development of Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD, Australia; bFaculty of Veterinary Sciences, Bangladesh Agricultural University, Mymensingh, Bangladesh ABSTRACT ARTICLE HISTORY Whipworms are parasitic nematodes that live in the gut of more than 500 million people world- Received 19 April 2017 wide. Owing to the difficulty in obtaining parasite material, the mouse whipworm Trichuris muris Accepted 7 January 2018 has been extensively used as a model to study human whipworm infections. These nematodes KEYWORDS secrete a multitude of compounds that interact with host tissues where they orchestrate a parasitic extracellular vesicles; existence. Herein we provide the first comprehensive characterization of the excretory/secretory exosomes; Trichuris muris; products of T. muris. We identify 148 proteins secreted by T. muris and show for the first time that whipworm; miRNA; the mouse whipworm secretes exosome-like extracellular vesicles (EVs) that can interact with host proteomics; organoids cells. We use an Optiprep® gradient to purify the EVs, highlighting the suitability of this method for purifying EVs secreted by a parasitic nematode. We also characterize the proteomic and genomic content of the EVs, identifying >350 proteins, 56 miRNAs (22 novel) and 475 full-length mRNA transcripts mapping to T. muris gene models. Many of the miRNAs putatively mapped to mouse genes are involved in regulation of inflammation, implying a role in parasite-driven immunomo- dulation. In addition, for the first time to our knowledge, colonic organoids have been used to demonstrate the internalization of parasite EVs by host cells. Understanding how parasites interact with their host is crucial to develop new control measures. This first characterization of the proteins and EVs secreted by T. muris provides important information on whipworm–host communication and forms the basis for future studies. Introduction adult worms, the rodent whipworm, Trichuris muris, has been extensively used as a tractable model of Infections with soil-transmitted helminths (STH) affect human trichuriasis [3–5]. In addition to parasitologists, more than 1.5 billion people worldwide, causing great immunologists have also benefited from the study of T. socio-economic impact as well as physical and intellec- muris infections, and a significant amount of basic tual retardation [1]. Among the STH, hookworms immunology research has been conducted using this (Necator americanus and Ancylostoma duodenale), model (reviewed by [6]). For instance, the role of IL-13 roundworms (Ascaris lumbricoides) and whipworms in resistance to nematode infections was elucidated (Trichuris trichiura) are of particular importance, using T. muris [7]. owing to their high prevalence and disease burden in The recent publication of the genome and transcrip- impoverished countries [2]. For instance, T. trichiura tome of T. muris has provided meaningful insights into alone infects around 500 million people worldwide, the immunobiology of whipworm infections [8]. This and contributes to 638,000 years of life lived with work provided new information on potential drug targets disability (YLDs) [2]. against trichuriasis and elucidated important traits that Infection with Trichuris spp. occurs after ingestion drive chronicity. Despite this progress, and the tractability of infective eggs, which hatch in the caecum of the of the T. muris model, very few proteomic studies have host. Larvae penetrate the mucosal tissue, where they been conducted, and only a handful of reports have moult to become adult worms and reside for the rest of described proteins secreted by Trichuris spp. [9–14]. their lives. Owing to the difficulty in obtaining parasite Drake et al. characterized a pore-forming protein that material to study whipworm infections, particularly T. muris [14]andT. trichiura [13] use to drill holes in CONTACT Javier Sotillo [email protected]; Alex Loukas [email protected] Centre for Biodiscovery and Molecular Development of Therapeutics, James Cook University, Cairns, Queensland 4878, Australia *These authors contributed equally to this work. Supplemental data for this article can be accessed here. © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 R. M. EICHENBERGER ET AL. the host cell membrane. Furthermore, it has been sug- 37°C and 5% CO2. Each well contained ~500 worms in gested that a thioredoxin-like protein secreted by the pig 4.5 ml media. The media obtained during the first 4 h whipworm Trichuris suis plays a role in mucosal home- after parasite culturing were discarded for further analy- ostasis [11]. sis. Dead worms were removed, and ES products were The importance of excretory/secretory (ES) products collected daily, subjected to sequential differential centri- in governing host–parasite interactions and ensuring fugation at 500 g,2000g and 4000 g for 30 min each to parasite survival in inhospitable environments is indis- remove eggs and parasite debris. For the isolation of ES putable. Traditionally, ES products were believed to con- products, media were concentrated using a 10 kDa spin tain only soluble proteins, lipids, carbohydrates and concentrator (Merck Millipore, Burlington, MA, USA) genomic content; however, the recent discovery of extra- and stored at 1.0 mg/ml in PBS at −80°C until required. cellular vesicles (EVs) secreted by helminths has revealed For the isolation of EVs, the media obtained after a new paradigm in the study of host–parasite relation- differential centrifugation were processed as described ships [15–17]. Helminth EVs have immunomodulatory previously [21]. Briefly, ES products were concentrated effects and contribute to pathogenesis. For instance, EVs using a 10 kDa spin concentrator, followed by centrifuga- secreted by parasitic flatworms can promote tumorigen- tion for 45 min at 12,000 g to remove larger vesicles. A esis [18] and polarize host macrophages towards a M1 MLS-50 rotor (Beckman Coulter, Brea, CA, USA) was phenotype [19], while EVs from the gastrointestinal used to ultracentrifuge the supernatant for 3 h at nematode Heligmosomoides polygyrus contain small 120,000 g, and the resultant pellet was resuspended in RNAs that can modulate host innate immunity [20]. 70 μl of PBS and subjected to Optiprep® discontinous In the present study, we aim to characterize the gradient (ODG) separation. One millilitre of 40%, 20%, factors involved in T. muris–host relationships. We 10% and 5% iodixanol solutions prepared in 0.25 M provide the first proteomic analysis of the soluble pro- sucrose, 10 mM Tris-HCl, pH 7.2, was layered in decreas- teins present in the ES products, and we describe the ing density in an ultracentrifuge tube, and the 70 µl con- proteomic and nucleic acid content of EVs secreted by taining the resuspended EVs was added to the top layer whipworms. This work provides important informa- and ultracentrifuged at 120,000 g for 18 h at 4°C. Seventy tion on whipworm biology and contributes to the microlitres of PBS was added to the control tube prepared development of new strategies and targets to combat as described above. A total of 12 fractions were recovered nematode infections in humans and animals. from the ODG, and the excess Optiprep® solution was removed by buffer exchanging with 8 ml of PBS contain- ing 1× EDTA-free protease inhibitor cocktail (Santa Experimental procedures Cruz, Dallas, TX, USA) using a 10 kDa spin concentrator. Ethics statement The absorbance (340 nm) was measured in each of the fractions, and density was calculated using a standard The study was approved by the James Cook University curve with known standards. The protein concentration (JCU) Animal Ethics Committee (A2213). Mice were of all fractions was measured using a Pierce BCA Protein maintained at the JCU animal house (Cairns campus) Assay Kit (ThermoFischer, Waltham, MA, USA). All under normal conditions of regulated temperature (22° fractions were kept at −80°C until use. C) and lighting (12 h light/dark cycle) with free access to pelleted food and water. The mice were kept in cages in compliance with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes. Size and concentration analysis of EVs The size distribution and particle concentration of fractions recovered after ODG were measured using Parasite material, isolation of ES products and EV tunable resistive pulse sensing (TRPS) by qNano purification (Izon, Christchurch, New Zealand) following the man- Parasites were obtained from genetically susceptible B10. ufacturer’s instructions. Voltage and pressure values BR mice infected with 200 T. muris eggs. The infection were set to optimize the signal to ensure high sensitiv- load
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