断奶应激对五指山猪仔猪肠道形态、抗氧化能力及Nrf2信号通路的影响

doi:10.16431/j.cnki.1671-7236.2025.05.010

Abstract

Abstract: 【Objective】 The purpose of this study was to analyze the changes of intestinal morphology,antioxidant capacity and other related indexes of Wuzhishan piglets after weaning,and explore the mechanism of Nrf2 signaling pathway on intestinal oxidative stress in early weaned piglets.【Method】 Forty-eight 35-day-old Wuzhishan piglets of similar weight (4.43 kg±0.58 kg) and good body condition were selected and divided into 4 groups with 12 piglets in each group.They were slaughtered and collected samples on the day of weaning (0 d),and the 3rd,7th and 10th days after weaning,respectively.The intestinal morphology,blood antioxidant-related enzyme activity,the reactive oxygen species (ROS) level in intestinal mucosa,intestinal Nrf2 signaling pathway and the expression of antioxidant enzyme-related gene of piglets in each group were detected.【Result】 Compared with weaning 0 days,①On the 3rd day after weaning,the villus height of duodenum in piglets was significantly decreased (P＜0.05),and the development trend of jejunum was similar to that of duodenum.The villus height and villus height/crypt depth were significantly increased on the 7th day after weaning (P＜0.05).②The activity of glutathione peroxidase (GSH-Px) of serum in piglets was significantly decreased (P＜0.05).The total antioxidant capacity (T-AOC) showed an upward trend after weaning,and reached the highest level on the 7th day after weaning (P＜0.05).The malondialdehyde (MDA) content in serum showed a slow downward trend after weaning (P＞0.05),and significantly increased on the 10th day after weaning (P＜0.05).③The ROS level in small intestinal mucosa of piglets was significantly increased on the 3rd and 7th days after weaning (P＜0.05),and there was no significant change on the 10th day after weaning (P＞0.05).④The expression of SOD1,SOD2,GPx1 and GPx4 genes in jejunum of piglets were significantly decreased on the 7th day after weaning (P＜0.05).The expression of SOD2 gene in ileum of piglets was significantly decreased on the 7th day after weaning (P＜0.05),and the expression of GPx4 and CAT genes in ileum of piglets were significantly increased on the 10th day after weaning (P＜0.05).⑤The expression of Nrf2 gene in ileum of piglets was significantly increased on the 10th day after weaning (P＜0.05).The expression of NQO1 gene in jejunum of piglets was significantly decreased on the 7th day after weaning (P＜0.05).The expression of HO-1 gene in duodenum of piglets was significantly decreased on the 3rd and 10th days after weaning (P＜0.05),and the expression of HO-1 gene in ileum of piglets was significantly increased on the 7th and 10th days after weaning (P＜0.05).【Conclusion】 Weaning stress could significantly increase the ROS level in small intestine of weaned Wuzhishan piglets,causing oxidative stress,which could cause obvious intestinal morphological changes such as villus shedding,shortening and crypt hyperplasia in weaned Wuzhishan piglets.Oxidative stress caused by weaning could also be alleviated by up-regulating antioxidant enzyme activity and intestinal related gene expression in serum of piglets.

Key words: weaned piglets; intestinal morphology; oxidative stress; antioxidant capacity; Nrf2 signaling pathway

CLC Number:

S815.7

YU Miao, LI Yanjiao, ZHAO Yanling, CHAO Zhe, WANG Feng, LI Menghan, JIANG Zhiqiang, ZHANG Ting, XUE Xinyu, REN Zili, SUN Ruiping. Effects of Weaning Stress on Intestinal Morphology, Antioxidant Capacity and Nrf2 Signaling Pathway of Wuzhishan Piglets[J]. China Animal Husbandry and Veterinary Medicine, 2025, 52(5): 2045-2055.

References

[1] NOVAIS A K,DESCHÊNE K,MARTEL-KENNES Y,et al.Weaning differentially affects mitochondrial function,oxidative stress,inflammation and apoptosis in normal and low birth weight piglets[J]. PLoS One,2021,16(2):e0247188.
[2] HU C H,XIAO K,LUAN Z S,et al.Early weaning increases intestinal permeability,alters expression of cytokine and tight junction proteins,and activates mitogen-activated protein kinases in pigs[J]. Journal of Animal Science,2013,91(3):1094-1101.
[3] 王啸春.氧自由基对大鼠小肠上皮细胞的损伤及硫辛酸的干预研究[D].上海：上海交通大学，2011.WANG X C.Oxidative injury of free radical on the rat iecs and intervention by α-lipoic acid[D].Shanghai:Shanghai Jiao Tong University,2011.(in Chinese)
[4] YUAN S B,CHEN D W,ZHANG K Y,et al.Effects of oxidative stress on growth performance,nutrient digestibilities and activities of antioxidative enzymes of weanling pigs[J]. Asian-Australasian Journal of Animal Sciences,2007,20(10):1600-1605.
[5] RAME T,ERNEST S,GENEVIEVE M,et al.Oxidative stress and mitochondrial functions in the intestinal Caco-2/15 cell line[J].PLoS One,2010,5(7):e11817.
[6] XIAO D F,YUAN D X,TAN B H,et al.The role of Nrf2 signaling pathway in Eucommia ulmoides flavones regulating oxidative stress in the intestine of piglets[J].Oxi-dative Medicine and Cellular Longevity,2019,2019：9719618.
[7] ZHENG P,YU B,HE J,et al.Arginine metabolism and its protective effects on intestinal health and functions in weaned piglets under oxidative stress induced by diquat[J].British Journal of Nutrition,2017,117(11):1495-1502.
[8] CAO S T,WU H,WANG C C,et al.Diquat-induced oxidative stress increases intestinal permeability,impairs mitochondrial function,and triggers mitophagy in piglets[J].Journal of Animal Science,2018,96(5):1795-1805.
[9] SONG Z H,TONG G,XIAO K,et al.L-cysteine protects intestinal integrity,attenuates intestinal inflammation and oxidant stress,and modulates NF-B and Nrf2 pathways in weaned piglets after LPS challenge[J].Innate Immunity,2016,22(3):152-161.
[10] LI Y,ZHAO X L,JIANG X M,et al.Effects of dietary supplementation with exogenous catalase on growth performance,oxidative stress,and hepatic apoptosis in weaned piglets challenged with lipopolysaccharide[J].Journal of Animal Science,2020,98(3):skaa067.
[11] 葛雨竹，喻礼怀，董丽.断奶仔猪氧化应激模型的建立及其营养调控的研究进展[J].中国饲料，2019，19：19-23.GE Y Z,YU L H,DONG L.Research progress on modeling oxidative stress in weaned piglets and its nutritional regulation[J].China Feed,2019,19:19-23.(in Chinese)
[12] SUZUKI T,MOTOHASHI H,YAMAMOTO M.Toward clinical application of the Keap1-Nrf2 pathway[J]. Trends in Pharmacological Sciences,2013,34(6):340-346.
[13] 任晓丽，皇甫和平，米俊宪，等.槲皮素通过Nrf2信号通路缓解LPS诱导的牛乳腺上皮细胞氧化应激[J].中国兽医学报，2023，43(12)：2590-2596.REN X L,HUANGFU H P,MI J X,et al.Quercetin alleviates LPS-induced oxidative stress in bovine mammary epithelial cells through the Nrf2 signaling pathway[J].Chinese Journal of Veterinary Science,2023,43(12):2590-2596.(in Chinese)
[14] 张婷.五指山猪仔猪早期断奶应激对肠道免疫性能及肠道微生物影响的研究[D].乌鲁木齐：新疆农业大学,2023.ZHANG T.Effects of early weaning stress on intestinal immune performance and intestinal microorganism of Wuzhishan piglets[D].Urumqi:Xinjiang Agricultural University,2023.(in Chinese)
[15] 薛新宇.五指山猪肠道发育规律分析及屎肠球菌、精胺对其断奶仔猪肠道功能的影响[D].南宁：广西大学，2024.XUE X Y.Analysis of intestinal development of Wuzhishan pigs and effects of Enterococcus faecium and spermine on intestinal function of weaned[D].Nanning:Guangxi University,2024.(in Chinese)
[16] 陈凤鸣，陈佳亿，彭伟，等.氧化应激对猪肠道损伤机制的研究进展[J].动物营养学报，2018，30(8)：2887-2893.CHEN F M,CHEN J Y,PENG W,et al.Research progress on the mechanism of intestinal damage in pigs by oxidative stress[J].Chinese Journal of Animal Nutrition,2018,30(8):2887-2893.(in Chinese)
[17] 王磊.断奶仔猪肠道形态变化规律及其营养调控[D].长沙：湖南师范大学，2021.WANG L.Intestinal morphological changes and nutritional regulation of weaned piglets[D].Changsha:Hunan Normal University,2021.(in Chinese)
[18] ZHU L H,ZHAO K L,CHEN X L,et al.Impact of weaning and an antioxidant blend on intestinal barrier function and antioxidant status in pigs[J].Journal of Animal Science,2012,90(8):2581-2589.
[19] 李慧敏.4-萜品醇对氧化应激断奶仔猪生长性能及肠道损伤的调节作用[D].扬州：扬州大学，2023.LI H M.Effects of terpen-4-ol on growth performance and intestinal damage in weaned piglets with oxidative stress[D].Yangzhou:Yangzhou University,2023.(in Chinese)
[20] BHAGAT J,INGOLE B S,SINGH N.Glutathione S-transferase,catalase,superoxide dismutase,glutathione peroxidase,and lipid peroxidation as biomarkers of oxidative stress in snails:A review[J].Invertebrate Survival Journal,2016,13:336-349.
[21] 杨新露.α-硫辛酸对绵羊生长性能、抗氧化能力和免疫功能的影响及其机制研究[D].郑州：河南农业大学，2023.YANG X L.Effects of α-lipoic acid on growth performance,antioxidant capacity and immune function in sheep and its mechanism[D].Zhengzhou:Henan Agricultural University,2023.(in Chinese)
[22] CICALĂU P I G,CIAVOI G,SCROBOTĂ I,et al.Assessing the antioxidant benefits of topical carvacrol and magnolol periodontal hydrogel therapy in periodontitis associated with diabetes in Wistar rats[J].Dentistry Journal,2023,11(12):284.
[23] YIN J,WU M M,XIAO H,et al.Development of an antioxidant system after early weaning in piglets[J].Journal of Animal Science,2014,92(2):612-619.
[24] LIU S,ZHU Y,YAN S,et al.Phenethyl isothiocyanate induces IPEC-J2 cells cytotoxicity and apoptosis via S-G2/M phase arrest and mitochondria-mediated Bax/Bcl-2 pathway[J].Comparative Biochemistry and Physiology,Part C,2019,226：108574.
[25] 陈凤鸣,陈佳亿,李颖慧,等.霉菌毒素介导的氧化应激研究进展[J].动物营养学报,2019,31(9):3944-3952.CHEN F M,CHEN J Y,LI Y H,etc.Research progress of oxidative stress mediated by mycotoxins[J].Chinese Journal of Animal Nutrition,2019,31(9):3944-3952.(in Chinese)
[26] WANG L,JIANG L，CHU Y,et al.Dietary taurine improves growth performance and intestine health via the GSH/GSSG antioxidant system and Nrf2/ARE signaling pathway in weaned piglets[J].Antioxidants,2023,12(10):1852.
[27] 陈刚.止痢草油缓解断奶仔猪肠道氧化应激的作用及机制[D].武汉：华中农业大学，2015.CHEN G.Effect and mechanism of oregano essential oil reduce intestinal oxidative stress in weaned pigs[D].Wuhan:Huazhong Agricultural University,2015.(in Chinese)
[28] 盛永帅.断奶仔猪肠道UCP2表达与肠道发育的关系及NAC的调控作用[D].上海:上海交通大学,2015.SHENG Y S.The relationship between uncoupling protein 2 expression and gut development in weaned piglets and regulation effects of N-acetyl cysteine[D].Shanghai:Shanghai Jiao Tong University,2015.(in Chinese)
[29] MAYENGBAM P,MAJUMDER S,ALI M A,et al.Stress and antioxidative status of Zovawk piglets at different intervals of weaning[J].The Indian Journal of Animal Sciences,2022，92(4):513-516.
[30] 符清瑶.白藜芦醇对氧化应激仔猪生长性能和肠道健康的作用机制研究[D].海口：海南大学，2022.FU Q Y.Mechanism of resveratrol on growth performance and gut health of oxidatively stressed piglets[D].Haikou:Hainan University,2022.(in Chinese)
[31] TONELLI C,CHIO I I C,TUVESON D A.Transcriptional regulation by Nrf2[J].Antioxidants & Redox Signaling,2018,29(17):1727-1745.
[32] MENG Q,GUO T,LI G,et al.Dietary resveratrol improves antioxidant status of sows and piglets and regulates antioxidant gene expression in placenta by Keap1-Nrf2 pathway and Sirt1[J].Journal of Animal Science and Biotechnology,2018,9：34.
[33] 潘鹏.白藜芦醇通过Nrf2信号通路提高猪骨骼肌抗氧化能力的作用及其机制[D].南宁：广西大学，2021.PAN P.Research on the effect and mechanism of resveratrol on improving antioxidat capacity of porcine skeletal muscle through Nrf2 signaling pathway[D].Nanning:Guangxi University,2021.(in Chinese)
[34] LEE J M,SHIH A Y,MURPHY T H,et al.NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex Ⅰ inhibitors and increased concentrations of intracellular calcium in primary cortical neurons[J].Journal of Biological Chemistry,2003,278(39):37948-37956.

Effects of Weaning Stress on Intestinal Morphology, Antioxidant Capacity and Nrf2 Signaling Pathway of Wuzhishan Piglets

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