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Disruption of Gut Integrity and Permeability Contributes to Enteritis

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Disruption of Gut Integrity and Permeability Contributes to Enteritis Sitjà‑Bobadilla et al. Parasites Vectors (2019) 12:486 https://doi.org/10.1186/s13071‑019‑3746‑7 Parasites & Vectors RESEARCH Open Access Disruption of gut integrity and permeability contributes to enteritis in a fsh‑parasite model: a story told from serum metabolomics Ariadna Sitjà‑Bobadilla1,2* , Rubén Gil‑Solsona3, Itziar Estensoro1†, M. Carla Piazzon1†, Juan Antonio Martos‑Sitcha4,5, Amparo Picard‑Sánchez1, Juan Fuentes6, Juan Vicente Sancho3, Josep A. Calduch‑Giner2,4, Félix Hernández2,3 and Jaume Pérez‑Sánchez2,4 Abstract Background: In the animal production sector, enteritis is responsible for serious economic losses, and intestinal parasitism is a major stress factor leading to malnutrition and lowered performance and animal production efciency. The efect of enteric parasites on the gut function of teleost fsh, which represent the most ancient bony vertebrates, is far from being understood. The intestinal myxozoan parasite Enteromyxum leei dwells between gut epithelial cells and causes severe enteritis in gilthead sea bream (Sparus aurata), anorexia, cachexia, growth impairment, reduced marketability and increased mortality. Methods: This study aimed to outline the gut failure in this fsh‑parasite model using a multifaceted approach and to fnd and validate non‑lethal serum markers of gut barrier dysfunction. Intestinal integrity was studied in parasitized and non‑parasitized fsh by immunohistochemistry with specifc markers for cellular adhesion (E‑cadherin) and tight junctions (Tjp1 and Cldn3) and by functional studies of permeability (oral administration of FITC‑dextran) and electro‑ physiology (Ussing chambers). Serum samples from parasitized and non‑parasitized fsh were analyzed using non‑tar‑ geted metabolomics and some signifcantly altered metabolites were selected to be validated using commercial kits. Results: The immunodetection of Tjp1 and Cldn3 was signifcantly lower in the intestine of parasitized fsh, while no strong diferences were found in E‑cadherin. Parasitized fsh showed a signifcant increase in paracellular uptake measured by FITC‑dextran detection in serum. Electrophysiology showed a decrease in transepithelial resistance in infected animals, which showed a diarrheic profle. Serum metabolomics revealed 3702 ions, from which the dif‑ ferential expression of 20 identifed compounds signifcantly separated control from infected groups in multivariate analyses. Of these compounds, serum inosine (decreased) and creatine (increased) were identifed as relevant and validated with commercial kits. Conclusions: The results demonstrate the disruption of tight junctions and the loss of gut barrier function, a metab‑ olomic profle of absorption dysfunction and anorexia, which further outline the pathophysiological efects of E. leei. Keywords: Myxozoa, Enteromyxum leei, Gilthead sea bream, Teleostei, Aquaculture, Pathophysiology, Tight junctions, Gut barrier, Electrophysiology, Metabolomics *Correspondence: [email protected] †Itziar Estensoro and M. Carla Piazzon contributed equally to this work 1 Fish Pathology Group, Instituto de Acuicultura Torre de la Sal (IATS‑CSIC), 12595 Ribera de Cabanes, Castellón, Spain Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sitjà‑Bobadilla et al. Parasites Vectors (2019) 12:486 Page 2 of 18 Background [16]. In advanced E. leei infections, the intestine displays Enteritis is the infammation of the intestine in its hypertrophy of the lamina propria-submucosa and loss of broader sense. In humans it can be due to viral, bac- the epithelial palisade structure, together with an intense terial or parasitic infections, induced by exogenous local infammatory response [16–19]. agents (radiation, medication, drug abuse, etc.), or due Several techniques have been proposed for studying to infammatory conditions such as Crohn’s disease or the morphology and physiology of fsh gut [20]. How- ulcerative colitis. Recent fndings also implicate enteric ever, most of these techniques are time consuming, or parasites such as Cryptosporidium parvum and Giardia expensive and require lethal samplings. In non-piscine duodenalis in the development of post-infectious com- hosts, non-lethal markers have been identifed to meas- plications such as irritable bowel syndrome and their ure gut barrier failure for some enteric pathogens, under impact on the neural control of gut functions [1]. In ani- feld conditions [21]. In humans, several biomarkers have mal production, enteritis is responsible for serious eco- been used to measure gut permeability and loss of barrier nomic losses, intestinal parasitism being a major stress integrity in intestinal diseases, but there remains a need factor leading to malnutrition and lowered performance to explore their use in assessing the efect of nutritional and production efciency of livestock and poultry [2]. factors on gut barrier function. Future studies should aim Furthermore, intestinal health is critically important to establish normal ranges of available biomarkers and for welfare and performance in animal production and their predictive value for gut health in human cohorts enteric diseases that cause gut barrier failure result in [22]. Metabolomics are emerging as a valuable tool to high economic losses. Common factors in most enteritis fnd biomarkers in many diseases, as the metabolome scenarios are not only the action of infammation play- includes all small molecules that are present in a bio- ers, but also the loss of the gut integrity. Intestinal mucus logical system and thus, metabolites serve as direct sig- and intercellular tight junctions (TJs) of the epithelial natures of the metabolic responses and perturbations in layer act together to maintain the integrity of the gut metabolic pathways and tightly correlate with a particu- barrier [3]. Te maintenance of the intestinal epithelial lar phenotype. Tese properties make the serum metabo- barrier is the essential function of the intestinal epithe- lome an attractive minimally invasive technique for the lial cells (IECs), and intraepithelial lymphocytes (IELs) identifcation of system phenotypic perturbations, espe- also have sentinel functions in the maintenance of the cially those disruptions due to pathogens [23, 24], and it mucosal barrier integrity [4]. An imbalance in the intes- has started to be used in aquaculture to identify biomark- tinal barrier structure can fare up into an uncontrollable ers indicative of physiological responses of living organ- immune reaction in the intestinal microenvironment or isms to environmental or culture conditions [25–27]. allow the unrestrained growth of microbiota, which leads Te aim of the present study was to outline the gut to various diseases. Tis loss increases the translocation failure resulting from a well-characterized enteric fsh- of bacterial antigens and stimulates infammation in the parasite model using a multifaceted approach (immu- intestine [5, 6]. nocytochemistry, electrophysiology, gut permeability Fish intestine plays various physiological functions that and metabolomics tools) and to fnd and validate serum go beyond digestion of food and nutrient absorption. It non-lethal markers of gut barrier dysfunction. Tus, is also an important immunological site with a key role serum samples from parasitized and non-parasitized fsh in protecting the animal from pathogenic insults. Tere- were frst analysed using non-targeted metabolomics and fore, its integrity is essential to guarantee fsh growth, some signifcantly altered metabolites were selected to be health and welfare [7]. Fish gut integrity has been stud- validated using commercial kits with further samples. ied mainly in relation to diferent dietary interventions that may cause enteritis or several degrees of gut mal- Methods functioning [8–13] and almost no data are available for Fish infection trials and samplings pathogen-induced enteritis [14]. However, fsh intestinal Juvenile specimens of gilthead sea bream (GSB) (Spa- parasitic infections not only cause direct mortalities, rus aurata) were obtained from commercial fsh farms but also morbidity, poor growth, higher susceptibility to and transported to IATS-CSIC facilities (Castellón, opportunistic pathogens and lower resistance to stress Spain). Before each trial, 20 fsh from each stock were [15]. Te intestinal myxozoan parasite Enteromyxum leei sacrifced and checked by qPCR (18S ribosomal RNA dwells between gut epithelial cells and causes severe des- gene) [28] and histology to be specifc pathogen free and quamative enteritis in gilthead sea bream (Sparus aurata) clinically healthy. Animals were acclimatized at least (Teleostei), producing anorexia, cachexia, growth impair- 6 weeks before any intervention and were always kept ment, reduced marketability and increased mortality in 5-µm-fltered sea water (37.5‰ salinity), with open Sitjà‑Bobadilla et al. Parasites Vectors (2019) 12:486 Page 3 of 18 fow and natural photoperiod at
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