journal article Open Access Mar 28, 2024

Fucoidan Supplementation Improves Antioxidant Capacity via Regulating the Keap1/Nrf2 Signaling Pathway and Mitochondrial Function in Low-Weaning Weight Piglets

Antioxidants Vol. 13 No. 4 pp. 407 · MDPI AG
View at Publisher Save 10.3390/antiox13040407
Abstract
Fucoidan (FC) is known for its antioxidant properties, but it has unclear effects and mechanisms on weaned piglets. Two experiments were conducted to determine the optimal FC dosage in piglet diets and its protective effect against lipopolysaccharide (LPS)-induced oxidative stress. In experiment one, 24 low weight weaned piglets were randomly assigned to four dietary treatments: a basal diet (FC 0), or a diet supplemented with 150 (FC 150), 300 (FC 300), or 600 mg/kg FC (FC 600). In experiment two, 72 low-weaning weight piglets were randomly allocated into four treatments: a basal diet (CON), or 300 mg/kg of fucoidan added to a basal diet challenged with LPS (100 µg LPS/kg body weight) or not. The results showed that FC treatments increased the G:F ratio, and dietary FC 300 reduced the diarrhea incidence and increased the plasma IGF-1 concentrations. In addition, FC 300 and FC 600 supplementation increased the plasma SOD activity and reduced the plasma MDA concentration. LPS challenge triggered a strong systemic redox imbalance and mitochondrial dysfunction. However, dietary FC (300 mg/kg) supplementation increased the activity of antioxidant enzymes, including SOD, decreased the MDA concentration in the plasma and liver, down-regulated Keap1 gene expression, and up-regulated Nrf2, CAT, MFN2, SDHA, and UQCRB gene expression in the liver. These results indicated that dietary fucoidan (300 mg/kg) supplementation improved the growth performance and antioxidant capacity of low-weaning weight piglets, which might be attributed to the modulation of the Keap1/Nrf2 signaling pathway and the mitochondrial function in the liver.
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References
55
[1]
Wang, L., Zhang, S., Johnston, L., Levesque, C., Yin, J., and Dong, B. (2022). A systematic review and meta-analysis of dietary fat effects on reproductive performance of sows and growth performance of piglets. J. Anim. Sci. Biotechnol., 13. 10.1186/s40104-021-00662-3
[2]
Mao "Effect of gestation dietary methionine-to-lysine ratio on methionine metabolism and antioxidant ability of high-prolific sows" Anim. Nutr. (2021) 10.1016/j.aninu.2021.02.006
[3]
Craig "Extended nursing and/or increased starter diet allowances for low weaning weight pigs" Asian-Australas. J. Anim. Sci. (2020) 10.5713/ajas.19.0511
[4]
Magowan "The performance response of pigs of different wean weights to ‘high’ or ‘low’ input dietary regimes between weaning and 20 weeks of age" Livest. Sci. (2011) 10.1016/j.livsci.2010.09.010
[5]
Collins "Post-weaning and whole-of-life performance of pigs is determined by live weight at weaning and the complexity of the diet fed after weaning" Anim. Nutr. (2017) 10.1016/j.aninu.2017.01.001
[6]
St-Pierre, B., Palencia, J., and Samuel, R. (2023). Impact of early weaning on development of the swine gut microbiome. Microorganisms, 11. 10.3390/microorganisms11071753
[7]
Yin "Hydrolysed yeast from Kluyveromyces fragilis improves plasma antioxidant efficiency and immunoglobulin concentration, and faecal microbiota of weaned piglets" Ital. J. Anim. Sci. (2023) 10.1080/1828051x.2023.2206414
[8]
Cai, L., Gao, G., Yin, C., Bai, R., Li, Y., Sun, W., Pi, Y., Jiang, X., and Li, X. (2023). The effects of dietary silybin supplementation on the growth performance and regulation of intestinal oxidative injury and microflora dysbiosis in weaned piglets. Antioxidants, 12. 10.3390/antiox12111975
[9]
Li "Effects of daidzein on antioxidant capacity in weaned pigs and IPEC-J2 cells" Anim. Nutr. (2022) 10.1016/j.aninu.2022.06.014
[10]
Novais, A., Deschene, K., Martel-Kennes, Y., Roy, C., Laforest, J., Lessard, M., Matte, J., and Lapointe, J. (2021). Weaning differentially affects mitochondrial function, oxidative stress, inflammation and apoptosis in normal and low birth weight piglets. PLoS ONE, 16. 10.1371/journal.pone.0247188
[11]
Yu, L., Li, H., Peng, Z., Ge, Y., Liu, J., Wang, T., Wang, H., and Dong, L. (2021). Early weaning affects liver antioxidant function in piglets. Animals, 11. 10.3390/ani11092679
[12]
Luo "Weaning induced hepatic oxidative stress, apoptosis, and aminotransferases through MAPK signaling pathways in piglets" Oxid. Med. Cell. Longev. (2016) 10.1155/2016/4768541
[13]
Guerbette "Mitochondrial function in intestinal epithelium homeostasis and modulation in diet-induced obesity" Mol. Metab. (2022) 10.1016/j.molmet.2022.101546
[14]
Canto "Mitochondrial stress management: A dynamic journey" Cell Stress (2018) 10.15698/cst2018.10.158
[15]
Zheng "Acute exposure to waterborne cadmium induced oxidative stress and immunotoxicity in the brain, ovary and liver of zebrafish" Aquat. Toxicol. (2016) 10.1016/j.aquatox.2016.09.012
[16]
Cai, L., Ming, D., Chen, W., Zhao, Y., Li, Y., Sun, W., Pi, Y., Jiang, X., and Li, X. (2024). Silybin alleviated hepatic injury by regulating redox balance, inflammatory response, and mitochondrial function in weaned piglets under paraquat-induced oxidative stress. Antioxidants, 13. 10.3390/antiox13030324
[17]
Zhou "Puerarin protects against acetaminophen-induced oxidative damage in liver through activation of the Keap1/Nrf2 signaling pathway" Food Sci. Nutr. (2023) 10.1002/fsn3.3609
[18]
Kobayashi "Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species" Adv. Enzym. Regul. (2006) 10.1016/j.advenzreg.2006.01.007
[19]
Wang, Y., Liu, B., Wu, P., Chu, Y., Gui, S., Zheng, Y., and Chen, X. (2022). Dietary selenium alleviated mouse liver oxidative stress and NAFLD induced by obesity by regulating the Keap1/Nrf2 Pathway. Antioxidants, 11. 10.3390/antiox11020349
[20]
Zhao, Y., Zheng, Y., Wang, J., Ma, S., Yu, Y., White, W., Yang, S., Yang, F., and Lu, J. (2018). Fucoidan extracted from undaria pinnatifida: Source for nutraceuticals/functional foods. Mar. Drugs, 16. 10.3390/md16090321
[21]
Wang "Antioxidant and anti-photoaging effects of a fucoidan isolated from Turbinaria ornata" Int. J. Biol. Macromol. (2023) 10.1016/j.ijbiomac.2022.11.164
[22]
Ji, Y., Jin, D., Qi, J., Wang, X., Zhang, C., An, P., Luo, Y., and Luo, J. (2022). Fucoidan protects against doxorubicin-induced cardiotoxicity by reducing oxidative stress and preventing mitochondrial function injury. Int. J. Mol. Sci., 23. 10.3390/ijms231810685
[23]
Fang "Effects of fucoidan on growth performance, immunity, antioxidant ability, digestive enzyme activity, and hepatic morphology in juvenile common carp (Cyprinus carpio)" Front. Mar. Sci. (2023) 10.3389/fmars.2023.1167400
[24]
Bolhuis "Effects of pre-weaning housing in a multi-suckling system on performance and carbohydrate absorption of relatively light and heavy piglets around weaning" Animal (2018) 10.1017/s1751731117002257
[25]
Chen "Lactobacillus delbrueckii ameliorates intestinal integrity and antioxidant ability in weaned piglets after a lipopolysaccharide challenge" Oxid. Med. Cell. Longev. (2020)
[26]
Jiang "Effects of a blend of essential oils and an enzyme combination on nutrient digestibility, ileum histology and expression of inflammatory mediators in weaned piglets" Animal (2015) 10.1017/s1751731114002444
[27]
Tang "Role of epidermal growth factor in regulation of intestinal health of weaned piglets" Chin. J. Anim. Nutr. (2021)
[28]
Feng "Ulva prolifera extract alleviates intestinal oxidative stress via Nrf2 signaling in weaned piglets challenged with hydrogen peroxide" Front. Immunol. (2020) 10.3389/fimmu.2020.599735
[29]
Bergeron "Feed supplementation with arginine and zinc on antioxidant status and inflammatory response in challenged weanling piglets" Anim. Nutr. (2017) 10.1016/j.aninu.2017.06.009
[30]
Larriestra "Pig characteristics associated with mortality and light exit weight for the nursery phase" Can. Vet. J. (2006)
[31]
McAlpine "Effect of the interaction of seaweed extracts containing laminarin and fucoidan with zinc oxide on the growth performance, digestibility and faecal characteristics of growing piglets" Brit. J. Nutr. (2014) 10.1017/s0007114513003280
[32]
Sweeney "Extracts of laminarin and laminarin/fucoidan from the marine macroalgal species laminaria digitata improved growth rate and intestinal structure in young chicks, but does not influence Campylobacter jejuni colonisation" Anim. Feed Sci. Technol. (2017) 10.1016/j.anifeedsci.2017.08.001
[33]
Yang, W., Chen, J., Guo, G., Wang, S., Peng, S., Gao, Z., Zhao, Z., Lan, R., and Yin, F. (2022). The effects of fucoidan dietary supplementation on growth performance, serum antioxidant capacity, immune function indices and intestinal morphology in weaned kids. Animals, 12. 10.3390/ani12050574
[34]
Tuller "Dietary influence of fucoidan supplementation on growth of lates calcarifer" Aquac. Res. (2014) 10.1111/are.12029
[35]
Sivagnanavelmurugan "Dietary effect of Sargassum wightii fucoidan to enhance growth, prophenoloxidase gene expression of Penaeus monodon and immune resistance to Vibrio parahaemolyticus" Fish Shellfish Immun. (2014) 10.1016/j.fsi.2014.05.037
[36]
Rattigan, R., Sweeney, T., Vigors, S., Thornton, K., Rajauria, G., and O’Doherty, J. (2019). The effect of increasing inclusion levels of a fucoidan-rich extract derived from Ascophyllum nodosum on growth performance and aspects of intestinal health of pigs post-weaning. Mar. Drugs, 17. 10.3390/md17120680
[37]
Walsh "Effect of dietary laminarin and fucoidan on selected microbiota, intestinal morphology and immune status of the newly weaned pig" Br. J. Nutr. (2013) 10.1017/s0007114513000834
[38]
Tang "Weaning stress and intestinal health of piglets: A review" Front. Immunol. (2022) 10.3389/fimmu.2022.1042778
[39]
Xu, X., Wei, Y., Hua, H., Jing, X., Zhu, H., Xiao, K., Zhao, J., and Liu, Y. (2022). Polyphenols sourced from Ilex latifolia thunb. relieve intestinal injury via modulating ferroptosis in weanling piglets under oxidative stress. Antioxidants, 11. 10.3390/antiox11050966
[40]
Pardo, Z., Fernandez-Figares, I., Lachica, M., Lara, L., Nieto, R., and Seiquer, I. (2021). Impact of heat stress on meat quality and antioxidant markers in iberian pigs. Antioxidants, 10. 10.3390/antiox10121911
[41]
Kumar, S., Wang, M., Liu, Y., Zhu, Z., Fahad, S., Qayyum, A., and Zhu, G. (2022). Vanadium stress alters sweet potato (Ipomoea batatas L.) growth, ros accumulation, antioxidant defense system, stomatal traits, and vanadium uptake. Antioxidants, 11. 10.3390/antiox11122407
[42]
Vega "Resveratrol partially prevents oxidative stress and metabolic dysfunction in pregnant rats fed a low protein diet and their offspring" J. Physiol. (2016) 10.1113/jp271543
[43]
Yang "Effects of dietary rosemary extract supplementation on growth performance, nutrient digestibility, antioxidant capacity, intestinal morphology, and microbiota of weaning pigs" J. Anim. Sci. (2021) 10.1093/jas/skab237
[44]
Wang, Y., Chen, X., Huang, Z., Chen, D., Yu, B., Yu, J., Chen, H., He, J., Luo, Y., and Zheng, P. (2020). Dietary ferulic acid supplementation improves antioxidant capacity and lipid metabolism in weaned piglets. Nutrients, 12. 10.3390/nu12123811
[45]
Han "IGF-1 concentrations after weaning in young sows fed different pre-mating diets are positively associated with piglet mean birth weight at subsequent farrowing" Animal (2021) 10.1016/j.animal.2020.100029
[46]
Xia "Probing the molecular regulation of lipopolysaccharide stress in piglet liver by comparative proteomics analysis" Electrophoresis (2018) 10.1002/elps.201700467
[47]
Zhang "Olive oil cake extract stabilizes the physiological condition of lipopolysaccharide-challenged piglets by reducing oxidative stress and inflammatory responses and modulating the ileal microbiome" Food Funct. (2021) 10.1039/d0fo03012k
[48]
Rishi "The liver in regulation of iron homeostasis" Am. J. Physiol. Gastr. L. (2017) 10.1152/ajpgi.00004.2017
[49]
Song "Effects of dietary supplementation with enzymatically treated artemisia annua on growth performance, intestinal morphology, digestive enzyme activities, immunity, and antioxidant capacity of heat-stressed broilers" Poult. Sci. (2018) 10.3382/ps/pex312
[50]
Ma, X., McKeen, T., Zhang, J., and Ding, W. (2020). Role and mechanisms of mitophagy in liver diseases. Cells, 9. 10.3390/cells9040837

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Published
Mar 28, 2024
Vol/Issue
13(4)
Pages
407
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Funding
National Natural Science Foundation of China Award: 32260850
the China Postdoctoral Science Foundation Award: 32260850
the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences Award: 32260850
Cite This Article
Chenggang Yin, Qingyue Bi, Wenning Chen, et al. (2024). Fucoidan Supplementation Improves Antioxidant Capacity via Regulating the Keap1/Nrf2 Signaling Pathway and Mitochondrial Function in Low-Weaning Weight Piglets. Antioxidants, 13(4), 407. https://doi.org/10.3390/antiox13040407