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Giardia hinders growth by disrupting nutrient metabolism independent of inflammatory enteropathy.

ABSTRACT: Giardia lamblia (Giardia) is among the most common intestinal pathogens in children in low- and middle-income countries (LMICs). Although Giardia associates with early-life linear growth restriction, mechanistic explanations for Giardia-associated growth impairments remain elusive. Unlike other intestinal pathogens associated with constrained linear growth that cause intestinal or systemic inflammation or both, Giardia seldom associates with chronic inflammation in these children. Here we leverage the MAL-ED longitudinal birth cohort and a model of Giardia mono-association in gnotobiotic and immunodeficient mice to propose an alternative pathogenesis of this parasite. In children, Giardia results in linear growth deficits and gut permeability that are dose-dependent and independent of intestinal markers of inflammation. The estimates of these findings vary between children in different MAL-ED sites. In a representative site, where Giardia associates with growth restriction, infected children demonstrate broad amino acid deficiencies, and overproduction of specific phenolic acids, byproducts of intestinal bacterial amino acid metabolism. Gnotobiotic mice require specific nutritional and environmental conditions to recapitulate these findings, and immunodeficient mice confirm a pathway independent of chronic T/B cell inflammation. Taken together, we propose a new paradigm that Giardia-mediated growth faltering is contingent upon a convergence of this intestinal protozoa with nutritional and intestinal bacterial factors.

SUBMITTER: Giallourou N

PROVIDER: S-EPMC10195804 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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Giardia hinders growth by disrupting nutrient metabolism independent of inflammatory enteropathy.

Giallourou Natasa N Arnold Jason J McQuade Elizabeth T Rogawski ETR Awoniyi Muyiwa M Becket Rose Viguna Thomas RVT Walsh Kenneth K Herzog Jeremy J Gulati Ajay S AS Carroll Ian M IM Montgomery Stephanie S Quintela Pedro Henrique PH Faust Angela M AM Singer Steven M SM Fodor Anthony A AA Ahmad Tahmeed T Mahfuz Mustafa M Mduma Esto E Walongo Thomas T Guerrant Richard L RL Balfour Sartor R R Swann Jonathan R JR Kosek Margaret N MN Bartelt Luther A LA

Nature communications 20230518 1

Giardia lamblia (Giardia) is among the most common intestinal pathogens in children in low- and middle-income countries (LMICs). Although Giardia associates with early-life linear growth restriction, mechanistic explanations for Giardia-associated growth impairments remain elusive. Unlike other intestinal pathogens associated with constrained linear growth that cause intestinal or systemic inflammation or both, Giardia seldom associates with chronic inflammation in these children. Here we levera ...[more]

PMID: 37202423

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Project description:BackgroundSparganosis is a worldwide food-borne parasitic disease caused by spargana infection, which infects the muscle of frogs and snakes as well as many tissues and organs in humans. There are currently no viable treatments for sparganosis. Understanding spargana's nutrition source and carbohydrate metabolism may be crucial for identifying its energy supply and establishing methods of treatment for sparganosis.MethodsUsing an amino acid analyzer and nutrient concentration detection kits, we assessed nutrient concentrations in the muscles of Fejervarya limnocharis and Pelophylax plancyi infected or not infected with spargana. Quantitative polymerase chain reaction (PCR) was used to quantify the major enzymes involved in five glucose metabolism pathways of spargana developing in vivo. We also used quantitative PCR to assess key enzymes and transcriptome sequencing to explore the regulation of carbohydrate metabolic pathways in vitro in response to different 24-h food treatments.ResultsInfected muscle tissues had considerably higher concentrations of glucogenic and/or ketogenic amino acids, glucose, and glycogen than non-infected muscle tissues. We discovered that the number of differentially expressed genes in Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis was larger in low-glucose than in other dietary groups. We examined differences in the expression of genes producing amino acid transporters, glucose transporters, and cathepsins in spargana grown in various nutritional environments. In the normal saline group, only the major enzymes in the tricarboxylic acid cycle (TCA), glycogenesis, and glycogenolysis pathways were expressed. The L-glutamine group had the greatest transcriptional levels of critical rate-limiting enzymes of gluconeogenesis and glycogenesis. Furthermore, the low-glucose group had the highest transcriptional levels of critical rate-limiting enzymes involved in the TCA, glycolytic, and glycogenolysis pathways. Surprisingly, when compared to the in vitro culturing groups, spargana developing in vivo exhibited higher expression of these critical rate-limiting enzymes in these pathways, with the exception of the pentose phosphate pathway.ConclusionsSpargana have a variety of nutritional sources, and there is a close relationship between nutrients and the carbohydrate metabolism pathways. It takes a multi-site approach to block nutrient absorption and carbohydrate metabolism pathways to provide energy to kill them.

Project description:We investigated the effect and interaction of lysolecithin (LPL) and nutrition level on growth performance, nutrient ileal digestibility, expression of growth-related genes and nutrient transporter genes in broilers. A total of 1280 one day old Ross 308 mixed sex chicks with an average body weight 42.23 ± 2.4 g were randomly allotted into 2 × 2 factorial arrangement (20 replicates per treatment and 16 chickens per replicate) with two types of diet (Normal nutrition treatments starter, grower and finisher diets with ME of 3000 kcal/kg, 3100 kcal/kg and 3200 kcal/kg, respectively, and CP level of 22%, 21%, and 20%, respectively; high nutrition treatments diets with 50 kcal/kg ME and 0.5% CP higher than normal nutrition treatment at each stage). Two levels of LPL supplementation (0 and 500 mg/kg) were also employed. From day 21 to day 35 and full stage of the experiment, the birds fed a high nutrition (HN) diet had a greater body weight gain (BWG) and lower feed conversion ratio (FCR) than those fed a normal nutrition (NN) diet (p < 0.05). Besides, lysolecithin increased BWG significantly (p < 0.05). The birds fed a diet with LPL revealed increasing fat digestibility compared to birds fed the basal diet (p < 0.05). LPL significantly increased the ileal digestibility of amino acids, including Ile, Thr, Phe, His, Arg, Tyr, Glu, Pro, Gly, Ala (p < 0.05). No interaction was found between LPL and nutrition level in BWG, FCR and nutrient digestibility. In HN diet, the genes expression of myogenic differentiation 1 (MYOD1), myogenin (MYOG), cluster of differentiation 36 (CD36), fatty acid-binding protein (FABP1), cationic amino acid transporter 1 (CAT1) and Y + L amino acid transporter 1 (y+, LAT1) were significantly elevated via LPL supplementation (p < 0.05). In NN diet, LPL significantly increased the genes expression of growth hormone (GH), insulin-like growth factor 1 (IGF1), MYOD1 and y+, LAT1 (p < 0.05). In conclusion, upregulating the nutrients transporter gene and growth-related gene expression of the host, independent of nutrition level changes, may be the action mechanism of lysolecithin on growth promotion in animals.

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Giardia hinders growth by disrupting nutrient metabolism independent of inflammatory enteropathy.

Publications

Giardia hinders growth by disrupting nutrient metabolism independent of inflammatory enteropathy.

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