Feeding Docosahexaenoic Acid and Arachidonic Acid during Suckling and Weaning Contributes to Oral Tolerance Development by Beneficially Modulating the Intestinal Cytokine and Immunoglobulin Levels in an Allergy-Prone Brown Norway Rat Model

IF 3.7 3区医学 Q2 NUTRITION & DIETETICS

Journal of Nutrition Pub Date : 2024-12-01 DOI:10.1016/j.tjnut.2024.10.021

Ren Wang, Dhruvesh Patel, Susan Goruk, Caroline Richard, Catherine J Field

{"title":"Feeding Docosahexaenoic Acid and Arachidonic Acid during Suckling and Weaning Contributes to Oral Tolerance Development by Beneficially Modulating the Intestinal Cytokine and Immunoglobulin Levels in an Allergy-Prone Brown Norway Rat Model","authors":"Ren Wang, Dhruvesh Patel, Susan Goruk, Caroline Richard, Catherine J Field","doi":"10.1016/j.tjnut.2024.10.021","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><div>Suckling and weaning arachidonic acid (ARA) + docosahexaenoic acid (DHA) supplementation promoted oral tolerance (OT) development in pups, however, the effect of it on the intestine to promote OT development remains unknown.</div></div><div><h3>Objective</h3><div>We aimed to explore the impact of this supplementation on intestinal fatty acid composition, structure, and indicators that are supportive of OT development.</div></div><div><h3>Methods</h3><div>Allergy-prone Brown Norway dams were randomly assigned to a control (0% ARA, 0% DHA) or ARA + DHA diet (0.45% ARA, 0.8% DHA) during suckling (0–3 wk). At weaning (3–8 wk), offspring were randomly assigned to a control (0% ARA, 0% DHA) or ARA + DHA diet (0.5% ARA, 0.5% DHA). At 3 wk, offspring in each group received an oral gavage of sucrose or ovalbumin (OVA) solution for five consecutive days. At 7 wk, all offspring received an intraperitoneal OVA injection. At 8 wk, offspring were terminated to evaluate jejunum morphology and measure mucosal food allergy-related secretory immunoglobulin A (sIgA) and cytokines, ileum phospholipid and triglyceride fatty acid compositions, and fecal calprotectin.</div></div><div><h3>Results</h3><div>Weaning ARA + DHA resulted in a higher percentage of DHA in ileum phospholipids and triglycerides (both <em>P</em> < 0.001), without affecting the percentage of ARA. Despite no lasting effect of suckling ARA + DHA on the DHA content in ileum phospholipids, a programming effect was found on the allergy-related intestinal immune profile [higher concentrations of mucosal IL-2 (<em>P</em> = 0.049) and sIgA (<em>P</em> = 0.033)]. OVA treatment resulted in a lower concentration of mucosal IL-6 (<em>P</em> = 0.026) regardless of dietary interventions. Offspring fed ARA + DHA during suckling and/or weaning had a higher concentration of mucosal transforming growth factor-beta (TGF-β) after OVA treatment but this was not observed in offspring fed control diets during suckling and weaning (<em>P</em> = 0.04).</div></div><div><h3>Conclusions</h3><div>Early life dietary ARA + DHA supplementation to allergy-prone rats enhanced the DHA concentration in intestinal phospholipids (weaning period) and increased the mucosal sIgA, IL-2, and TGF-β levels (suckling and weaning period), indicating its ability to create a tolerogenic intestinal environment to support OT development.</div></div>","PeriodicalId":16620,"journal":{"name":"Journal of Nutrition","volume":"154 12","pages":"Pages 3790-3802"},"PeriodicalIF":3.7000,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Nutrition","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0022316624010988","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NUTRITION & DIETETICS","Score":null,"Total":0}

引用次数: 0

Abstract

Background

Suckling and weaning arachidonic acid (ARA) + docosahexaenoic acid (DHA) supplementation promoted oral tolerance (OT) development in pups, however, the effect of it on the intestine to promote OT development remains unknown.

Objective

We aimed to explore the impact of this supplementation on intestinal fatty acid composition, structure, and indicators that are supportive of OT development.

Methods

Allergy-prone Brown Norway dams were randomly assigned to a control (0% ARA, 0% DHA) or ARA + DHA diet (0.45% ARA, 0.8% DHA) during suckling (0–3 wk). At weaning (3–8 wk), offspring were randomly assigned to a control (0% ARA, 0% DHA) or ARA + DHA diet (0.5% ARA, 0.5% DHA). At 3 wk, offspring in each group received an oral gavage of sucrose or ovalbumin (OVA) solution for five consecutive days. At 7 wk, all offspring received an intraperitoneal OVA injection. At 8 wk, offspring were terminated to evaluate jejunum morphology and measure mucosal food allergy-related secretory immunoglobulin A (sIgA) and cytokines, ileum phospholipid and triglyceride fatty acid compositions, and fecal calprotectin.

Results

Weaning ARA + DHA resulted in a higher percentage of DHA in ileum phospholipids and triglycerides (both P < 0.001), without affecting the percentage of ARA. Despite no lasting effect of suckling ARA + DHA on the DHA content in ileum phospholipids, a programming effect was found on the allergy-related intestinal immune profile [higher concentrations of mucosal IL-2 (P = 0.049) and sIgA (P = 0.033)]. OVA treatment resulted in a lower concentration of mucosal IL-6 (P = 0.026) regardless of dietary interventions. Offspring fed ARA + DHA during suckling and/or weaning had a higher concentration of mucosal transforming growth factor-beta (TGF-β) after OVA treatment but this was not observed in offspring fed control diets during suckling and weaning (P = 0.04).

Conclusions

Early life dietary ARA + DHA supplementation to allergy-prone rats enhanced the DHA concentration in intestinal phospholipids (weaning period) and increased the mucosal sIgA, IL-2, and TGF-β levels (suckling and weaning period), indicating its ability to create a tolerogenic intestinal environment to support OT development.

查看原文本刊更多论文

在易过敏的挪威褐大鼠模型中，在哺乳期和断奶期喂食二十二碳六烯酸和花生四烯酸可调节肠道细胞因子和免疫球蛋白水平，从而促进口腔耐受性的形成。

背景：吸吮和断奶时补充花生四烯酸（ARA）+二十二碳六烯酸（DHA）可促进幼犬口腔耐受性（OT）的发育，但其对肠道促进OT发育的影响仍然未知：我们的目的是探索补充 DHA 对肠道脂肪酸组成、结构和支持 OT 发育的指标的影响：方法：在哺乳期（0-3周），将易过敏的布朗挪威母牛随机分为对照组（0%ARA、0%DHA）或ARA+DHA组（0.45%ARA、0.8%DHA）。断奶时（3-8 周），后代被随机分配到对照组（0%ARA、0%DHA）或 ARA+DHA 日粮（0.5%ARA、0.5%DHA）中。3 周时，各组后代连续 5 天口服蔗糖或卵清蛋白（OVA）溶液。7 周时，所有后代腹腔注射 OVA。8周时，对后代进行终止饲养，以评估空肠形态，测量与食物过敏相关的粘膜sIgA和细胞因子、回肠磷脂和甘油三酯脂肪酸组成以及粪便钙蛋白：断奶后摄入 ARA+DHA 会导致回肠磷脂和甘油三酯中 DHA 的比例升高（均为 P）：给易过敏大鼠补充早期膳食 ARA+DHA 可提高肠道磷脂中的 DHA 含量（断奶期），并提高粘膜 sIgA、IL-2 和 TGF-β 的水平（哺乳期和断奶期），这表明 ARA+DHA 能够创造耐受性肠道环境，支持 OT 的发育。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Journal of Nutrition 医学-营养学

CiteScore

7.60

自引率

4.80%

发文量

260

审稿时长

39 days

期刊介绍： The Journal of Nutrition (JN/J Nutr) publishes peer-reviewed original research papers covering all aspects of experimental nutrition in humans and other animal species; special articles such as reviews and biographies of prominent nutrition scientists; and issues, opinions, and commentaries on controversial issues in nutrition. Supplements are frequently published to provide extended discussion of topics of special interest.