Reduced Glutathione Promoted Growth Performance by Improving the Jejunal Barrier, Antioxidant Function, and Altering Proteomics of Weaned Piglets
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animal Ethics Statement
2.2. Glutathione and Chlortetracycline
2.3. Animals and Experimental Design
2.4. Growth Performance
2.5. Slaughter and Tissue Sample Collection
2.6. Histochemistry Staining
2.7. Blood Biochemistry Index and Redox Capacity of the Jejunal Mucosa
2.8. Proteomics Analysis of the Jejunal Mucosa Through Four-Dimensional Data-Independent Acquisition (4D-DIA)–Mass Spectrometry (MS)
2.9. Quantitative Real-Time PCR (qRT-PCR)
2.10. Statistical Analysis
3. Results
3.1. Effects of Dietary GSH on Growth Performance in Weaned Piglets
3.2. Effects of Dietary GSH on Biochemical Parameters of Plasma in Weaned Piglets
3.3. Effects of Dietary GSH on Histomorphology and Epithelial Barrier of the Jejunal Mucosa in Weaned Piglets
3.4. Jejunal Antioxidant Capacity in Weaned Piglets
3.5. Proteomics and qRT-PCR Analysis Showed Dietary GSH2 Improved the Jejunal Redox Homeostasis of the Jejunal Mucosa in Weaned Piglets
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Ingredients | 6–11 kg | 11–25 kg |
---|---|---|
Corn | 35.31 | 47.55 |
Extruded corn | 15.00 | 13.00 |
Fermented soybean meal | 9.00 | 8.50 |
Soybean meal | —— | 9.00 |
Extruded soybean | 10.00 | 6.00 |
Fish meal | 4.00 | 4.00 |
Whey powder | 11.00 | 6.00 |
Soybean hull | 5.00 | —— |
Soybean oil | 1.20 | —— |
Plasma protein powder | 3.00 | —— |
White granulated sugar | 2.00 | 2.00 |
50% Choline chloride | 0.20 | 0.18 |
Sodium chloride | 0.45 | 0.45 |
Calcium hydrophosphate | 0.62 | 0.60 |
Limestone | 0.65 | 0.74 |
Zinc oxide | 0.30 | —— |
Copper sulfate | —— | 0.015 |
L-Lysine | 0.60 | 0.54 |
DL-Methionine | 0.22 | 0.2 |
L-Threonine | 0.21 | 0.21 |
L-Trptophan | 0.04 | 0.03 |
Premix compound A | 1.50 | 1.00 |
Total | 100.00 | 100.00 |
Nutrient levels B | ||
DE (MJ/kg) | 14.86 | 14.72 |
Crude protein | 19.20 | 19.10 |
Total calcium | 0.68 | 0.70 |
Total phosphorus | 0.56 | 0.53 |
STTD phosphorus | 0.39 | 0.34 |
SID Lysine | 1.57 | 1.41 |
SID Methionine + Cysteine | 0.89 | 0.81 |
SID Threonine | 0.97 | 0.88 |
SID Trptophan | 0.26 | 0.23 |
Appendix B
Gene | Primer Sequence (5′→3′) | Accession No. |
---|---|---|
β-Actin | Forward: CACGCCATCCTGCGTCTGGA | XM_003124280.4 |
Reverse: AGCACCGTGTTGGCGTAGAG | ||
ZO-1 | Forward: AGCCCGAGGCGTGTTT | XM_013993251.1 |
Reverse: GGTGGGAGGATGCTGTTG | ||
Claudin1 | Forward: AAATCAGAACTTTGGAGGC | NM_021101.4 |
Reverse: AAACAAGAGTGCTATGGGTC | ||
Occludin | Forward: GCACCCAGCAACGACAT | NM_001163647.2 |
Reverse: CATAGACAGAATCCGAATCAC | ||
Muc1 | Forward: CGCCTGCCTGAATCTGTT | NM_001018016.2 |
Reverse: GCTCTTGGTAGTAGTCGGTGC | ||
Muc2 | Forward: CTGCTCCGGGTCCTGTGGGA | XM_007465997.1 |
Reverse: CCCGCTGGCTGGTGCGATAC | ||
MLCK | Forward: CTCCAAGGACCGGATGAA | XM_001929078.6 |
Reverse: CCACTGAGCCCTGAGATCAT | ||
GPX4 | Forward: TGAGGCAAGACGGAGGTAAACT | NM_214407 |
Reverse: TCCGTAAACCACACTCAGCATATC | ||
Hsp70 | Forward: GCCCTGAATCCGCAGAATA | NM_001123127.1 |
Reverse: TCCCCACGGTAGGAAACG | ||
Hsp90 | Forward: AAGCCCTGAGAGACAACTCG | U94395.1 |
Reverse: TGAAGCCAGAAGACAGCAGA | ||
SIRT1 | Forward: GTTAGGAGGTGAATATGCCAAG | NM_001145750.2 |
Reverse: CAACTCTTTTTGTGTTCGTGGA | ||
FoxO1 | Forward: CCAGTCTTCACCAGGCACCA | NM_214014.3 |
Reverse: GCCTCCGTAACTCGATTTGCT | ||
Akt1 | Forward: TCATGCAGCACCGTTTCTT | NM_001159776.1 |
Reverse: AATACCTGGTGTCCGTCTCG | ||
β-Actin | Forward: CACGCCATCCTGCGTCTGGA | XM_003124280.4 |
Reverse: AGCACCGTGTTGGCGTAGAG | ||
ZO-1 | Forward: AGCCCGAGGCGTGTTT | XM_013993251.1 |
Reverse: GGTGGGAGGATGCTGTTG | ||
Claudin1 | Forward: AAATCAGAACTTTGGAGGC | NM_021101.4 |
Reverse: AAACAAGAGTGCTATGGGTC | ||
Occludin | Forward: GCACCCAGCAACGACAT | NM_001163647.2 |
Reverse: CATAGACAGAATCCGAATCAC | ||
Muc1 | Forward: CGCCTGCCTGAATCTGTT | NM_001018016.2 |
References
- Jayaraman, B.; Nyachoti, C.M. Husbandry practices and gut health outcomes in weaned piglets: A review. Anim. Nutr. 2017, 3, 205–211. [Google Scholar] [CrossRef] [PubMed]
- van der Meulen, J.; Koopmans, S.J.; Dekker, R.A.; Hoogendoorn, A. Increasing weaning age of piglets from 4 to 7 weeks reduces stress, increases post-weaning feed intake but does not improve intestinal functionality. Animal 2010, 4, 1653–1661. [Google Scholar] [CrossRef]
- Li, Z.; Liu, S.; Zhao, Y.; Wang, J.; Ma, X. Compound organic acid could improve the growth performance, immunity and antioxidant properties, and intestinal health by altering the microbiota profile of weaned piglets. J. Anim. Sci. 2023, 3, 101. [Google Scholar] [CrossRef] [PubMed]
- Stahly, T.S.; Cromwell, G.L.; Monegue, H.J. Effects of the dietary inclusion of copper and(or) antibiotics on the performance of weanling pigs. J. Anim. Sci. 1980, 51, 1347–1351. [Google Scholar] [CrossRef]
- Long, S.; Liu, S.; Wang, J.; Mahfuz, S.; Piao, X. Natural capsicum extract replacing chlortetracycline enhances performance via improving digestive enzyme activities, antioxidant capacity, anti-inflammatory function, and gut health in weaned pigs. Anim. Nutr. 2021, 7, 305–314. [Google Scholar] [CrossRef] [PubMed]
- Capps, K.M.; Amachawadi, R.G.; Menegat, M.B.; Woodworth, J.C.; Perryman, K.; Tokach, M.D.; Dritz, S.S.; DeRouchey, J.M.; Goodband, R.D.; Bai, J.; et al. Impact of added copper, alone or in combination with chlortetracycline, on growth performance and antimicrobial resistance of fecal enterococci of weaned piglets. J. Anim. Sci. 2020, 98, skaa003. [Google Scholar] [CrossRef]
- Chen, J.; Chen, D.; Yu, B.; Luo, Y.; Zheng, P.; Mao, X.; Yu, J.; Luo, J.; Huang, Z.; Yan, H.; et al. Chlorogenic acid attenuates oxidative stress-induced intestinal mucosa disruption in wweaned pigs. Front. Vet. Sci. 2022, 9, 806253. [Google Scholar]
- Su, J.; Zhu, Q.; Zhao, Y.; Han, L.; Yin, Y.; Blachier, F.; Wang, Z.; Kong, X. Dietary supplementation with Chinese Herbal residues or their fermented products modifies the colonic microbiota, bacterial metabolites, and expression of genes related to colon barrier function in weaned piglets. Front. Microbiol. 2018, 9, 3181. [Google Scholar] [CrossRef] [PubMed]
- Meng, Q.; Guo, T.; Li, G.; Sun, S.; He, S.; Cheng, B.; Shi, B.; Shan, A. Dietary resveratrol improves antioxidant status of sows and piglets and regulates antioxidant gene expression in placenta by Keap1-Nrf2 pathway and Sirt1. J. Anim. Sci. Biotechnol. 2018, 9, 34. [Google Scholar] [CrossRef] [PubMed]
- Van Le Thanh, B.; Lemay, M.; Bastien, A.; Lapointe, J.; Lessard, M.; Chorfi, Y.; Guay, F. The potential effects of antioxidant feed additives in mitigating the adverse effects of corn naturally contaminated with Fusarium mycotoxins on antioxidant systems in the intestinal mucosa, plasma, and liver in weaned pigs. Mycotoxin Res. 2016, 32, 99–116. [Google Scholar] [CrossRef]
- Lv, H.; Zhen, C.; Liu, J.; Yang, P.; Hu, L.; Shang, P. Unraveling the potential role of glutathione in multiple forms of cell death in cancer therapy. Oxid. Med. Cell. Longev. 2019, 2019, 3150145. [Google Scholar] [CrossRef]
- Haddad, J.J. Redox regulation of pro-inflammatory cytokines and IkappaB-alpha/NF-kappaB nuclear translocation and activation. Biochem. Biophys. Res. Commun. 2002, 296, 847–856. [Google Scholar] [CrossRef] [PubMed]
- Shen, H.; Wang, W. Effect of glutathione liposomes on diabetic nephropathy based on oxidative stress and polyol pathway mechanism. J. Liposome Res. 2021, 31, 317–325. [Google Scholar] [CrossRef] [PubMed]
- Asanuma, M.; Miyazaki, I. Glutathione and Related Molecules in Parkinsonism. Int. J. Mol. Sci. 2021, 22, 8689. [Google Scholar] [CrossRef]
- Labarrere, C.A.; Kassab, G.S. Glutathione deficiency in the pathogenesis of SARS-CoV-2 infection and its effects upon the host immune response in severe COVID-19 disease. Front. Microbiol. 2022, 13, 979719. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Manna, S.K.; Golla, S.; Krausz, K.W.; Cai, Y.; Garcia-Milian, R.; Chakraborty, T.; Chakraborty, J.; Chatterjee, R.; Thompson, D.C.; et al. Glutathione deficiency-elicited reprogramming of hepatic metabolism protects against alcohol-induced steatosis. Free Radic. Biol. Med. 2019, 143, 127–139. [Google Scholar] [CrossRef] [PubMed]
- Homma, T.; Fujii, J. Application of Glutathione as Anti-Oxidative and Anti-Aging Drugs. Curr. Drug Metab. 2015, 16, 560–571. [Google Scholar] [CrossRef] [PubMed]
- Estrada, E.; Rodriguez-Gil, J.E.; Rivera Del Alamo, M.M.; Pena, A.; Yeste, M. Effects of reduced glutathione on acrosin activity in frozen-thawed boar spermatozoa. Reprod. Fertil. Dev. 2017, 29, 283–293. [Google Scholar] [CrossRef]
- Li, F.; Cui, L.; Yu, D.; Hao, H.; Liu, Y.; Zhao, X.; Pang, Y.; Zhu, H.; Du, W. Exogenous glutathione improves intracellular glutathione synthesis via the gamma-glutamyl cycle in bovine zygotes and cleavage embryos. J. Cell. Physiol. 2019, 234, 7384–7394. [Google Scholar] [CrossRef]
- Xiang, X.; Wang, H.; Zhou, W.; Wang, C.; Guan, P.; Xu, G.; Zhao, Q.; He, L.; Yin, Y.; Li, T. Glutathione Protects against Paraquat-Induced Oxidative Stress by Regulating Intestinal Barrier, Antioxidant Capacity, and CAR Signaling Pathway in Weaned Piglets. Nutrients 2022, 15, 198. [Google Scholar] [CrossRef]
- Liang, C.; Ren, Y.; Tian, G.; He, J.; Zheng, P.; Mao, X.; Yu, J.; Yu, B. Dietary glutathione supplementation attenuates oxidative stress and improves intestinal barrier in diquat-treated weaned piglets. Arch. Anim. Nutr. 2023, 77, 141–154. [Google Scholar] [CrossRef]
- Wang, C.; Su, B.; Lu, S.; Han, S.; Jiang, H.; Li, Z.; Liu, Y.; Liu, H.; Yang, Y. Effects of Glutathione on Growth, Intestinal Antioxidant Capacity, Histology, Gene Expression, and Microbiota of Juvenile Triploid Oncorhynchus mykiss. Front. Physiol. 2021, 12, 784852. [Google Scholar] [CrossRef] [PubMed]
- National Research Council. Nutrient Requirements of Swine, 11th ed.; National Academies Press: Washington, DC, USA, 2012.
- Tian, Z.; Cui, Y.; Lu, H.; Ma, X. Effects of long-term feeding diets supplemented with Lactobacillus reuteri 1 on growth perfor mance, digestive and absorptive function of the small intestine in pigs. J. Funct. Foods 2020, 71, 104010. [Google Scholar] [CrossRef]
- St. Martin, C.C.; Eudoxie, G.D.; Black, K.C.; Brathwaite, R.A.; Lauckner, B. Assessing maturity of rotary barrel green waste composts for use as tomato and sweet pepper seedling starter and transplant growth substrates. Int. J. Veg. Sci. 2014, 20, 28–58. [Google Scholar] [CrossRef]
- Yin, J.; Wu, M.M.; Xiao, H.; Ren, W.K.; Duan, J.L.; Yang, G.; Li, T.J.; Yin, Y.L. Development of an antioxidant system after early weaning in piglets. J. Anim. Sci. 2014, 92, 612–619. [Google Scholar] [CrossRef]
- Smith, F.; Clark, J.E.; Overman, B.L.; Tozel, C.C.; Huang, J.H.; Rivier, J.E.; Blikslager, A.T.; Moeser, A.J. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298, 352–363. [Google Scholar] [CrossRef] [PubMed]
- Xun, W.; Shi, L.; Zhou, H.; Hou, G.; Cao, T.; Zhao, C. Effects of curcumin on growth performance, jejunal mucosal membrane integrity, morphology and immune status in weaned piglets challenged with enterotoxigenic Escherichia coli. Int. Immunopharmacol. 2015, 27, 46–52. [Google Scholar] [CrossRef] [PubMed]
- Nicholson, J.K.; Holmes, E.; Kinross, J.M.; Darzi, A.W.; Takats, Z.; Lindon, J.C. Metabolic phenotyping in clinical and surgical environments. Nature 2012, 491, 384–392. [Google Scholar] [CrossRef]
- Asantewaa, G.; Tuttle, E.T.; Ward, N.P.; Kang, Y.P.; Kim, Y.; Kavanagh, M.E.; Girnius, N.; Chen, Y.; Rodriguez, K.; Hecht, F.; et al. Glutathione synthesis in the mouse liver supports lipid abundance through NRF2 repression. Nat. Commun. 2024, 15, 6152. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Bai, J.; Zhou, Q.; Hu, Y.; Wang, Q.; Yang, L.; Chen, H.; An, H.; Zhou, C.; Wang, Y.; et al. Glutathione prevents high glucose-induced pancreatic fibrosis by suppressing pancreatic stellate cell activation via the ROS/TGFbeta/SMAD pathway. Cell Death Dis. 2022, 13, 440. [Google Scholar] [CrossRef] [PubMed]
- Piotrowska, A.; Burlikowska, K.; Szymeczko, R. Changes in blood chemistry in broiler chickens during the fattening period. Folia Biol. 2011, 59, 183–187. [Google Scholar] [CrossRef] [PubMed]
- Filipović, N.; Physiology, D.O. Changes in concentration and fractions of blood serum proteins of chickens during fattening. Vet. Arh. 2007, 77, 319–326. [Google Scholar]
- Lala, V.; Zubair, M.; Minter, D.A. Liver Function Tests. In StatPearls; StatPearls: Treasure Island, FL, USA, 2023. [Google Scholar]
- Ke, Y.; Wu, T.; Lei, X.; Zhang, C.; Zhou, J.; Li, J.; Zhang, H.; Chen, X.; Wang, J.; Wang, L. Reduced glutathione ameliorates liver function, oxidative stress and inflammation after interventional therapy for hepatocellular carcinoma. J. BUON 2020, 25, 1361–1367. [Google Scholar] [PubMed]
- Wang, M.; Hu, Q.; Wang, N.; Jiang, Y.; Dong, T.; Cao, S.; Zhou, A. Glutathione attenuates copper levels and alleviates hepatic injury in TX mice. Biol. Trace Elem. Res. 2024, 24, 1–9. [Google Scholar] [CrossRef] [PubMed]
- LiverTox. Tetracyclines. In LiverTox: Clinical and Research Information on Drug-Induced Liver Injury; National Institute of Diabetes and Digestive and Kidney Diseases: Bethesda, MD, USA, 2019. [Google Scholar]
- Miller, D.L.; Hanson, W.; Schedl, H.P.; Osborne, J.W. Proliferation rate and transit time of mucosal cells in small intestine of the diabetic rat. Gastroenterology 1977, 73, 1326–1332. [Google Scholar] [CrossRef] [PubMed]
- Wang, K.; Yang, A.; Peng, X.; Lv, F.; Wang, Y.; Cui, Y.; Wang, Y.; Zhou, J.; Si, H. Linkages of various calcium sources on immune performance, diarrhea rate, intestinal barrier, and post-gut microbial structure and function in piglets. Front. Nutr. 2022, 9, 921773. [Google Scholar] [CrossRef] [PubMed]
- Biasato, I.; Ferrocino, I.; Colombino, E.; Gai, F.; Schiavone, A.; Cocolin, L.; Vincenti, V.; Capucchio, M.T.; Gasco, L. Effects of dietary Hermetia illucens meal inclusion on cecal microbiota and small intestinal mucin dynamics and infiltration with immune cells of weaned piglets. J. Anim. Sci. Biotechnol. 2020, 11, 64. [Google Scholar] [CrossRef]
- McShane, A.; Bath, J.; Jaramillo, A.M.; Ridley, C.; Walsh, A.A.; Evans, C.M.; Thornton, D.J.; Ribbeck, K. Mucus. Curr. Biol. 2021, 31, 938–945. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Xiao, S.; Gong, Z.; Zhu, X.; Yang, Q.; Li, Y.; Gao, S.; Dong, Y.; Shi, Z.; Wang, Y.; et al. Wuji Wan formula ameliorates diarrhea and disordered colonic motility in post-inflammation irritable bowel syndrome rats by modulating the gut microbiota. Front. Microbiol. 2017, 8, 2307. [Google Scholar] [CrossRef]
- El Gazzar, W.B.; Sliem, R.E.; Bayoumi, H.; Nasr, H.E.; Shabanah, M.; Elalfy, A.; Radwaan, S.E.; Gebba, M.A.; Mansour, H.M.; Badr, A.M.; et al. Melatonin alleviates intestinal barrier damaging effects induced by polyethylene microplastics in Albino rats. Int. J. Mol. Sci. 2023, 24, 13619. [Google Scholar] [CrossRef] [PubMed]
- de Oliveira, A.P.; Perles, J.; de Souza, S.R.G.; Sestak, S.S.; da Motta Lima, F.G.; Almeida, G.; Cicero, L.R.; Clebis, N.K.; Guarnier, F.A.; Blegniski, F.P.; et al. L-glutathione 1% promotes neuroprotection of nitrergic neurons and reduces the oxidative stress in the jejunum of rats with Walker-256-bearing tumor. Neurogastroenterol. Motil. 2023, 35, e14688. [Google Scholar] [CrossRef] [PubMed]
- Goncalves, E.; Poulos, R.C.; Cai, Z.; Barthorpe, S.; Manda, S.S.; Lucas, N.; Beck, A.; Bucio-Noble, D.; Dausmann, M.; Hall, C.; et al. Pan-cancer proteomic map of 949 human cell lines. Cancer Cell 2022, 40, 835–849. [Google Scholar] [CrossRef] [PubMed]
- Kaszubowska, L.; Foerster, J.; Kaczor, J.J.; Schetz, D.; Slebioda, T.J.; Kmiec, Z. NK cells of the oldest seniors represent constant and resistant to stimulation high expression of cellular protective proteins SIRT1 and HSP70. Immun. Ageing 2018, 15, 12. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.B.; Lee, S.H.; Um, J.H.; Oh, W.K.; Kim, D.W.; Kang, C.D.; Kim, S.H. Sensitization of multidrug-resistant human cancer cells to Hsp90 inhibitors by down-regulation of SIRT1. Oncotarget 2015, 6, 36202–36218. [Google Scholar] [CrossRef] [PubMed]
- Hori, Y.S.; Kuno, A.; Hosoda, R.; Horio, Y. Regulation of FOXOs and p53 by SIRT1 modulators under oxidative stress. PLoS ONE 2013, 8, e73875. [Google Scholar] [CrossRef] [PubMed]
- Song, S.; Chu, L.; Liang, H.; Chen, J.; Liang, J.; Huang, Z.; Zhang, B.; Chen, X. Protective effects of dioscin against doxorubicin-induced hepatotoxicity via regulation of Sirt1/FOXO1/NF-kappab signal. Front. Pharmacol. 2019, 10, 1030. [Google Scholar] [CrossRef] [PubMed]
- Ren, B.C.; Zhang, Y.F.; Liu, S.S.; Cheng, X.J.; Yang, X.; Cui, X.G.; Zhao, X.R.; Zhao, H.; Hao, M.F.; Li, M.D.; et al. Curcumin alleviates oxidative stress and inhibits apoptosis in diabetic cardiomyopathy via Sirt1-Foxo1 and PI3K-Akt signalling pathways. J. Cell. Mol. Med. 2020, 24, 12355–12367. [Google Scholar] [CrossRef]
- Cheng, Q.; Chen, M.; Liu, M.; Chen, X.; Zhu, L.; Xu, J.; Xue, J.; Wu, H.; Du, Y. Semaphorin 5A suppresses ferroptosis through activation of PI3K-AKT-mTOR signaling in rheumatoid arthritis. Cell Death Dis. 2022, 13, 608. [Google Scholar] [CrossRef] [PubMed]
- Chen, K.; Xue, R.; Geng, Y.; Zhang, S. Galangin inhibited ferroptosis through activation of the PI3K/AKT pathway in vitro and in vivo. FASEB J. 2022, 36, e22569. [Google Scholar] [CrossRef]
- Zhang, Y.; Swanda, R.V.; Nie, L.; Liu, X.; Wang, C.; Lee, H.; Lei, G.; Mao, C.; Koppula, P.; Cheng, W.; et al. mTORC1 couples cyst(e)ine availability with GPX4 protein synthesis and ferroptosis regulation. Nat. Commun. 2021, 12, 1589. [Google Scholar] [CrossRef]
- Liu, J.; Yang, G.; Zhang, H. Glyphosate-triggered hepatocyte ferroptosis via suppressing Nrf2/GSH/GPX4 axis exacerbates hepatotoxicity. Sci. Total Environ. 2023, 862, 160839. [Google Scholar] [CrossRef] [PubMed]
- Cui, J.; Zhou, Q.; Yu, M.; Liu, Y.; Teng, X.; Gu, X. 4-tert-butylphenol triggers common carp hepatocytes ferroptosis via oxidative stress, iron overload, SLC7A11/GSH/GPX4 axis, and ATF4/HSPA5/GPX4 axis. Ecotoxicol. Environ. Saf. 2022, 242, 113944. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Sun, B.; Zhang, S.; Li, J.; Qi, J.; Bai, C.; Zhang, J.; Liang, S. Glycine alleviates fluoride-induced oxidative stress, apoptosis and senescence in a porcine testicular Sertoli cell line. Reprod. Domest. Anim. 2021, 56, 884–896. [Google Scholar] [CrossRef]
- Salyha, N.; Salyha, Y. Protective role of l-glutamic acid and l-cysteine in mitigation the chlorpyrifos-induced oxidative stress in rats. Environ. Toxicol. Pharmacol. 2018, 64, 155–163. [Google Scholar] [CrossRef] [PubMed]
- Wu, B.W.; Wu, M.S.; Liu, Y.; Lu, M.; Guo, J.D.; Meng, Y.H.; Zhou, Y.H. SIRT1-mediated deacetylation of NF-kappaB inhibits the MLCK/MLC2 pathway and the expression of ET-1, thus alleviating the development of coronary artery spasm. Am. J. Physiol. Heart Circ. Physiol. 2021, 320, 458–468. [Google Scholar] [CrossRef] [PubMed]
- Jia, Z.Y.; Xia, Y.; Tong, D.; Yao, J.; Chen, H.Q.; Yang, J. Module-based functional pathway enrichment analysis of a protein-protein interaction network to study the effects of intestinal microbiota depletion in mice. Mol. Med. Rep. 2014, 9, 2205–2212. [Google Scholar] [CrossRef] [PubMed]
- Stage, T.B.; Graff, M.; Wong, S.; Rasmussen, L.L.; Nielsen, F.; Pottegard, A.; Brosen, K.; Kroetz, D.L.; Khojasteh, S.C.; Damkier, P. Dicloxacillin induces CYP2C19, CYP2C9 and CYP3A4 in vivo and in vitro. Br. J. Clin. Pharmacol. 2018, 84, 510–519. [Google Scholar] [CrossRef] [PubMed]
- Basso, A.D.; Solit, D.B.; Munster, P.N.; Rosen, N. Ansamycin antibiotics inhibit Akt activation and cyclin D expression in breast cancer cells that overexpress HER2. Oncogene 2002, 21, 1159–1166. [Google Scholar] [CrossRef]
- Zhang, X.; Chen, B.; Wu, J.; Sha, J.; Yang, B.; Zhu, J.; Sun, J.; Hartung, J.; Bao, E. Aspirin enhances the protection of Hsp90 from heat-stressed injury in cardiac microvascular endothelial cells through PI3K-Akt and PKM2 pathways. Cells 2020, 9, 243. [Google Scholar] [CrossRef]
- GB/T 6432-2018; Determination of crude Protein in Feeds—Kjeldahl Method. Ministry of Agriculture of the People’s Republic of China. China Agriculture Press: Beijing, China, 2018.
- GB/T 6436-2018; Determination of Calcium in Feeds. Ministry of Agriculture of the People’s Republic of China. China Agriculture Press: Beijing, China, 2018.
- GB/T 6437-2018; Determination of Phosphorus in Feeds—Spectrophotometry. Ministry of Agriculture of the People’s Republic of China. China Agriculture Press: Beijing, China, 2018.
- Feed Database in China. Tables of Feed Composition and Nutritive Values in China. 2020. Available online: https://www.chinafeeddata.org.cn/admin/Login/slcfb. (accessed on 31 December 2020).
Item | Treatments B | SEM | p-Value A | ||||||
---|---|---|---|---|---|---|---|---|---|
ABX | CON | GSH1 | GSH2 | GSH3 | ANOVA | Linear | Quadratic | ||
Body weight, kg | |||||||||
21 d | 6.63 | 6.63 | 6.63 | 6.63 | 6.63 | 0.01 | 0.968 | 0.981 | 0.98 |
35 d | 10.87 a | 10.26 b | 10.82 a | 10.88 a | 10.35 ab | 0.13 | 0.030 | 0.038 | 0.872 |
49 d | 16.38 a | 15.01 c | 16.11 ab | 16.65 a | 15.27 bc | 0.28 | 0.007 | 0.010 | 0.830 |
Days 1 to 14 | |||||||||
ADG, g | 302.77 a | 259.13 b | 299.17 a | 303.55 a | 265.20 ab | 9.24 | 0.001 | 0.005 | 0.836 |
ADFI, g | 373.97 | 362.72 | 387.63 | 397.81 | 369.15 | 6.38 | 0.139 | 0.016 | 0.591 |
F/G, g/g | 1.24 | 1.42 | 1.31 | 1.31 | 1.41 | 0.03 | 0.074 | 0.352 | 0.648 |
Days 15 to 28 | |||||||||
ADG, g | 393.30 a | 339.51 b | 378.13 a | 411.83 a | 351.79 ab | 12.35 | 0.001 | 0.002 | 0.546 |
ADFI, g | 555.52 | 532.16 | 568.50 | 595.00 | 539.33 | 11.18 | 0.137 | 0.022 | 0.455 |
F/G, g/g | 1.42 | 1.57 | 1.51 | 1.46 | 1.57 | 0.02 | 0.361 | 0.517 | 0.971 |
Days 1 to 28 | |||||||||
ADG, g | 348.04 a | 299.327 b | 338.65 a | 357.69 a | 308.496 ab | 10.14 | 0.001 | 0.002 | 0.785 |
ADFI, g | 464.753 ab | 447.44 b | 478.07 ab | 496.41 a | 454.24 b | 8.75 | 0.048 | 0.006 | 0.422 |
F/G, g/g | 1.34 | 1.50 | 1.42 | 1.39 | 1.49 | 0.02 | 0.078 | 0.335 | 0.872 |
Item | Treatments B | SEM | p-Value A | ||||||
---|---|---|---|---|---|---|---|---|---|
ABX | CON | GSH1 | GSH2 | GSH3 | ANOVA | Linear | Quadratic | ||
Triglyceride (mmol/L) | 0.35 ab | 0.30 b | 0.36 ab | 0.48 a | 0.32 ab | 0.03 | 0.034 | 0.006 | 0.155 |
Cholesterol (mmol//L) | 2.12 ab | 1.91 b | 2.04 ab | 2.53 a | 2.12 ab | 0.10 | 0.062 | 0.018 | 0.387 |
LDLC (mmol//L) | 1.77 | 1.61 | 1.64 | 1.49 | 1.68 | 0.05 | 0.498 | 0.278 | 0.186 |
HDLC (mmol//L) | 0.82 | 0.96 | 0.77 | 0.91 | 0.82 | 0.04 | 0.491 | 0.556 | 0.114 |
Glucose (mM/L) | 3.84 ab | 4.51 a | 3.77 ab | 3.26 b | 4.30 a | 0.22 | 0.001 | <0.001 | 0.365 |
Total protein (g/L) | 49.36 | 49.82 | 50.33 | 53.56 | 49.91 | 0.76 | 0.467 | 0.142 | 0.283 |
Albumin (g/L) | 32.98 b | 38.62 a | 34.53 ab | 39.00 a | 32.09 b | 1.43 | 0.006 | 0.63 | <0.001 |
Urea nitrogen (mmol/L) | 14.27 ab | 13.02 ab | 15.74 ab | 17.03 a | 11.62 b | 0.96 | 0.016 | 0.012 | 0.110 |
AST (U/L) | 36.14 a | 20.03 b | 11.75 bc | 17.34 bc | 7.14 c | 4.95 | <0.001 | <0.001 | 0.163 |
ALT (U/L) | 17.09 | 17.75 | 17.69 | 18.60 | 15.86 | 0.45 | 0.714 | 0.607 | 0.244 |
AST/ALT | 2.28 a | 1.15 b | 0.66 bc | 0.94 bc | 0.46 c | 0.31 | <0.001 | 0.001 | <0.001 |
AKP (U/L) | 168.32 | 174.38 | 175.18 | 184.35 | 156.66 | 4.57 | 0.675 | 0.530 | 0.235 |
Accession | Protein Description | Gene Name | FC | p-Value |
---|---|---|---|---|
GSH2 vs. CON | ||||
A0A287BL83 | Carbonyl reductase (NADPH) | NADPH | 0.56 | 0.010 |
A0A5G2QH97 | Voltage-dependent anion-selective channel protein 3 | VDAC3 | 0.66 | 0.037 |
P51781 | Glutathione S-transferase alpha M14 | GSTAM14 | 0.57 | 0.001 |
A0A0K1TQQ0 | Microsomal glutathione S-transferase 2 | MGST2 | 0.41 | 0.019 |
A0A287B452 | Voltage-dependent anion-selective channel protein 2 | VDAC2 | 0.29 | 0.003 |
A0A287BGN0 | Cytochrome c oxidase subunit | COX6A1 | 0.38 | 0.001 |
P04175 | NADPH-cytochrome P450 reductase | POR | 0.56 | 0.015 |
F1SDB7 | Flavin-containing monooxygenase | FMO5 | 0.66 | 0.009 |
Q29092 | Endoplasmin heat shock protein 90 kDa beta member 1 | Hsp90B1 | 1.69 | 0.004 |
A0A5G2R0T1 | Heat shock protein family A (Hsp70) member 4 | HspA4 | 2.67 | 0.047 |
P36968 | Phospholipid hydroperoxide glutathione peroxidase | GPX4 | 1.51 | 0.001 |
A7LKB1 | NAD-dependent protein deacetylase sirtuin-1 isoform a | SIRT1 | 1.56 | 0.000 |
A4L7N3 | Forkhead box protein O1 | FOXO1 | 1.57 | 0.002 |
A0A287B2S5 | Non-specific serine/threonine protein kinase | Akt1 | 1.52 | 0.028 |
GSH2 vs. ABX | ||||
A0A287B452 | Voltage-dependent anion-selective channel protein 2 | VDAC2 | 0.46 | 0.015 |
A0A287BGN0 | Cytochrome c oxidase subunit | COX6A1 | 0.44 | 0.004 |
A0A287BL83 | Carbonyl reductase (NADPH) | NADPH | 0.53 | 0.019 |
A0A5K1UL95 | Aldo-keto reductase family 1, member C1 | AKR1C3 | 0.43 | 0.045 |
P51781 | Glutathione S-transferase alpha M14 | GSTAM14 | 0.52 | 0.043 |
P81693 | Low molecular weight phosphortyrosine protein phosphatase | ACP1 | 2.97 | 0.017 |
A0A287BP39 | Cytochrome P450 2C42 | CYP2C42 | 0.57 | 0.039 |
F1S6B7 | Flavin-containing monooxygenase | FMO4 | 0.63 | 0.046 |
I6L6E1 | Aldehyde dehydrogenase | ALDH3B1 | 0.66 | 0.046 |
P04175 | NADPH-cytochrome P450 reductase | POR | 0.60 | 0.039 |
Q29092 | Endoplasmin | Hsp90B1 | 1.73 | 0.005 |
A0A5G2R0T1 | Heat shock protein family A (Hsp70) member 4 | HspA4 | 2.80 | 0.041 |
P36968 | Phospholipid hydroperoxide glutathione peroxidase | GPX4 | 1.51 | 0.002 |
A7LKB1 | NAD-dependent protein deacetylase sirtuin-1 isoform a | SIRT1 | 1.57 | 0.002 |
A4L7N3 | Forkhead box protein O1 | FOXO1 | 1.56 | 0.001 |
A0A287B2S5 | Non-specific serine/threonine protein kinase | Akt1 | 1.52 | <0.0001 |
ABX vs. CON | ||||
A0A287ANH8 | H (+)-transporting two-sector ATPase | ATPase | 0.65 | 0.037 |
A0A287BMK6 | Cytochrome P450 family 4 subfamily F member 3 | CYP4F3 | 4.16 | 0.021 |
F1SC62 | Cytochrome P450 2C42 | CYP2C42 | 2.12 | 0.017 |
A0A287B2S5 | Non-specific serine/threonine protein kinase | Akt1 | 0.08 | <0.0001 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tian, Z.; Cui, Y.; Yu, M.; Deng, D.; Li, Z.; Ma, X.; Qu, M. Reduced Glutathione Promoted Growth Performance by Improving the Jejunal Barrier, Antioxidant Function, and Altering Proteomics of Weaned Piglets. Antioxidants 2025, 14, 107. https://doi.org/10.3390/antiox14010107
Tian Z, Cui Y, Yu M, Deng D, Li Z, Ma X, Qu M. Reduced Glutathione Promoted Growth Performance by Improving the Jejunal Barrier, Antioxidant Function, and Altering Proteomics of Weaned Piglets. Antioxidants. 2025; 14(1):107. https://doi.org/10.3390/antiox14010107
Chicago/Turabian StyleTian, Zhimei, Yiyan Cui, Miao Yu, Dun Deng, Zhenming Li, Xianyong Ma, and Mingren Qu. 2025. "Reduced Glutathione Promoted Growth Performance by Improving the Jejunal Barrier, Antioxidant Function, and Altering Proteomics of Weaned Piglets" Antioxidants 14, no. 1: 107. https://doi.org/10.3390/antiox14010107
APA StyleTian, Z., Cui, Y., Yu, M., Deng, D., Li, Z., Ma, X., & Qu, M. (2025). Reduced Glutathione Promoted Growth Performance by Improving the Jejunal Barrier, Antioxidant Function, and Altering Proteomics of Weaned Piglets. Antioxidants, 14(1), 107. https://doi.org/10.3390/antiox14010107