Proteome changes induced by a short, non-cytotoxic exposure to the mycoestrogen zearalenone in the pig intestine

Soler, Laura; Stella, Alexandre; Seva, Juan; Pallarés, F. J.; Lahjouji, Tarek; Burlet‐Schiltz, Odile; Oswald, Isabelle P.

doi:10.1016/j.jprot.2020.103842

Cited by 12 publications

(8 citation statements)

References 63 publications

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“…A study indicated that ZEA (6 and 8 μg/mL) induced cytochrome oxidoreductase-dependent oxidative stress in intestinal epithelial cells in gilts and the death of IPEC-J2 cells, following activation of the p38/MAPK signal pathway to regulate autophagy [ 44 ]. Furthermore, another study demonstrated that ZEA (100 μmoL) can induce the production of ERα signals and the destruction of signal cascade components such as NF-κB, ERK1/2, dcdx2, and HIF1α in the intestine of pigs [ 45 ]. However, the specific molecular mechanisms underlying the estrogenic activity of ZEA associated with intestinal toxicity need to be further verified.…”

Section: Resultsmentioning

confidence: 99%

Effects of Dietary Zearalenone Exposure on the Growth Performance, Small Intestine Disaccharidase, and Antioxidant Activities of Weaned Gilts

Liu

Yang

et al. 2020

Animals

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Zearalenone (ZEA) is a secondary metabolite with estrogenic effects produced by Fusarium fungi and mainly occurs as a contaminant of grains such as corn and wheat. ZEA, to which weaned gilts are extremely sensitive, is the main Fusarium toxin detected in corn–soybean meal diets. Our aim was to examine the effects of ZEA on the growth performance, intestinal disaccharidase activity, and anti-stress capacity of weaned gilts. Twenty 42-day-old healthy Duroc × Landrace × Large White weaned gilts (12.84 ± 0.26 kg) were randomly divided into control and treatment (diet containing 1.04 mg/kg ZEA) groups. The experiment included a 7-day pre-trial period followed by a 35-day test period, all gilts were euthanized and small intestinal samples were collected and subjected to immunohistochemical and western blot analyses. The results revealed that inclusion of 1.04 mg/kg ZEA in the diet significantly reduced the activities of lactase, sucrase, and maltase in the duodenum, jejunum, and ileum of gilts. Similarly, the activities of superoxide dismutase and glutathione peroxidase in the duodenum, jejunum, and ileum, and activities of catalase in the jejunum and ileum were reduced (p < 0.05). Conversely, the content of malondialdehyde in the duodenum, jejunum, and ileum, and the integrated optical density (IOD), IOD in single villi, and the mRNA and protein expression of heat shock protein 70 (Hsp70) were significantly increased (p < 0.05). The results of immunohistochemical analyses revealed that the positive reaction of Hsp70 in the duodenum, jejunum, and ileum of weaned gilts was enhanced in the ZEA treatment, compared with the control. The findings of this study indicate the inclusion of ZEA (1.04 mg/kg) in the diet of gilts reduced the activity of disaccharidase enzymes and induced oxidative stress in the small intestine, thereby indicating that ZEA would have the effect of reducing nutrient absorption in these animals.

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Section: Resultsmentioning

confidence: 99%

Effects of Dietary Zearalenone Exposure on the Growth Performance, Small Intestine Disaccharidase, and Antioxidant Activities of Weaned Gilts

Liu

Yang

et al. 2020

Animals

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“…ZEN is a relatively well-known natural ED [8]. Many of the toxic effects of ZEN derive from its binding to estrogen receptors, but other non-classical estrogen triggered pathways can also be activated by ZEN [22], including the ability to change the circulating levels of important metabolic-related hormones such as gonadotropins, insulin, and estrogen [23,24]. The latter effects are known to mediate the metabolic disruption induced by xenoestrogens [25].…”

Section: Discussionmentioning

confidence: 99%

“…The levels of circulating adipokines reflect the metabolic status of an individual and are altered in the case of exposure to MDCs [21]. Although the impact that ZEN could have in the levels of circulating adipokines has not been studied to date, research data suggest that ZEN could disturb the expression and function of adipokines through the dysregulation of PPARα, PPARγ [17] as well as ERK1/2 and PI3K/Akt [22] signaling pathways.…”

Section: Introductionmentioning

confidence: 99%

Exposure to Zearalenone Leads to Metabolic Disruption and Changes in Circulating Adipokines Concentrations in Pigs

Nagl¹,

Grenier²,

Pinton

et al. 2021

Toxins

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Zearalenone (ZEN) is a mycotoxin classified as an endocrine disruptor. Many endocrine disruptors are also metabolic disruptors able to modulate energy balance and inflammatory processes in a process often involving a family of protein hormones known as adipokines. The aim of our study was to elucidate the role of ZEN as metabolic disruptor in pigs by investigating the changes in energy balance and adipokines levels in response to different treatment diets. To this end, weaned piglets (n = 10/group) were exposed to either basal feed or feed contaminated with 680 and 1620 µg/kg ZEN for 28 days. Serum samples collected at days 7 and 21 were subjected to biochemistry analysis, followed by determination of adipokine levels using a combined approach of protein array and ELISA. Results indicate that ZEN has an impact on lipid and glucose metabolism that was different depending on the dose and time of exposure. In agreement with these changes, ZEN altered circulating adipokines concentrations, inducing significant changes in adiponectin, resistin, and fetuin B. Our results suggest that ZEN may function as a natural metabolism-disrupting chemical.

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“…Moreover, a study in vitro also reported that 100 μM ZEN promoted the development of intestinal pathology in castrated male pigs by activating Wnt/β-catenin signaling and inhibiting TGF-β [ 17 ]. The overall process of toxin action on cells or tissues is usually accompanied by changes in genomics, metabolomics, and proteomics [ 18 , 19 ]. Solar et al [ 19 ] explored the proteome changes induced by a short, non-cytotoxic exposure to ZEN in the intestine using pig jejunal explants and indicated that ZEN could alter epithelial homeostasis through regulating a cascade of highly inter-connected signaling events essential for the small intestinal crypt–villus cycle.…”

Section: Introductionmentioning

confidence: 99%

Quantitative Proteomic Analysis of Zearalenone-Induced Intestinal Damage in Weaned Piglets

Jiang²,

Lü³

et al. 2022

Toxins

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Zearalenone (ZEN), also known as the F-2 toxin, is a common contaminant in cereal crops and livestock products. This experiment aimed to reveal the changes in the proteomics of ZEN-induced intestinal damage in weaned piglets by tandem mass spectrometry tags. Sixteen weaned piglets either received a basal diet or a basal diet supplemented with 3.0 mg/kg ZEN in a 32 d study. The results showed that the serum levels of ZEN, α-zearalenol, and β-zearalenol were increased in weaned piglets exposed to ZEN (p < 0.05). Zearalenone exposure reduced apparent nutrient digestibility, increased intestinal permeability, and caused intestinal damage in weaned piglets. Meanwhile, a total of 174 differential proteins (DEPs) were identified between control and ZEN groups, with 60 up-regulated DEPs and 114 down-regulated DEPs (FC > 1.20 or <0.83, p < 0.05). Gene ontology analysis revealed that DEPs were mainly involved in substance transport and metabolism, gene expression, inflammatory, and oxidative stress. The Kyoto Encyclopedia of Genes and Genomes analysis revealed that DEPs were significantly enriched in 25 signaling pathways (p < 0.05), most of which were related to inflammation and amino acid metabolism. Our study provides valuable clues to elucidate the possible mechanism of ZEN-induced intestinal injury.

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Proteome changes induced by a short, non-cytotoxic exposure to the mycoestrogen zearalenone in the pig intestine

Cited by 12 publications

References 63 publications

Effects of Dietary Zearalenone Exposure on the Growth Performance, Small Intestine Disaccharidase, and Antioxidant Activities of Weaned Gilts

Effects of Dietary Zearalenone Exposure on the Growth Performance, Small Intestine Disaccharidase, and Antioxidant Activities of Weaned Gilts

Exposure to Zearalenone Leads to Metabolic Disruption and Changes in Circulating Adipokines Concentrations in Pigs

Quantitative Proteomic Analysis of Zearalenone-Induced Intestinal Damage in Weaned Piglets

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