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Potential protective effects of sodium butyrate on glycinin-induced oxidative stress, inflammatory response, and growth inhibition in Cyprinus carpio

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Abstract

Investigated mitigating effects of sodium butyrate (SB) on the inflammatory response, oxidative stress, and growth inhibition of common carp (Cyprinus carpio) (2.94 ± 0.2 g) are caused by glycinin. Six isonitrogenous and isoenergetic diets were prepared, in which the basal diet was the control diet and the Gly group diet contained 80 g/kg glycinin, while the remaining 4 diets were supplemented with 0.75, 1.50, 2.25, and 3.00 g/kg SB, respectively. The feeding trial lasted for 8 weeks, and the results indicated that supplementing the diet with 1.50–2.25 g/kg of SB significantly improved feed efficiency and alleviated the growth inhibition induced by glycinin. Hepatopancreas and intestinal protease activities and the content of muscle crude protein were significantly decreased by dietary glycinin, but supplement 1.50–2.25 g/kg SB partially reversed this result. SB (1.50–2.25 g/kg) increased the activities of aspartate aminotransferase (AST) and alanine aminotransferase (ALT) in the hepatopancreas and reduced the activities of AST and ALT in the serum. Glycinin significantly reduced immune and antioxidant enzyme activities, whereas 1.50–2.25 g/kg SB reversed these adverse effects. Furthermore, compared with the Gly group, supplement 1.50–2.25 g/kg SB eminently up-regulated the TGF-β and IL-10 mRNA, and down-regulated the IL-1β, TNF-α, and NF-κB mRNA in hepatopancreas, mid-intestine (MI), and distal intestine (DI). Meanwhile, supplement 1.50–2.25 g/kg SB activated the Keap1-Nrf2-ARE signaling pathway and upregulate CAT, SOD, and HO-1 mRNA expression in hepatopancreas, MI, and DI. Summarily, glycinin induced inflammatory response, and oxidative stress of common carp ultimately decreased the digestive function and growth performance. SB partially mitigated these adverse effects by activating the Keap1-Nrf2-ARE signaling pathway and inhibiting the NF-κB signaling pathway.

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Data availability

The data supporting the results of this study are available from the corresponding author upon request.

References

  • Abdel-Latif HMR, Abdel-Tawwab M, Dawood MAO et al (2020) Benefits of dietary butyric acid, sodium butyrate, and their protected forms in aquafeeds: a review[J]. Reviews in Fisheries Science & Aquaculture 28(4):421–448

    Article  Google Scholar 

  • Abdel-Tawwab M, Shukry M, Farrag FA et al (2021) Dietary sodium butyrate nanoparticles enhanced growth, digestive enzyme activities, intestinal histomorphometry, and transcription of growth-related genes in Nile tilapia juveniles[J]. Aquaculture 536:736467

    Article  CAS  Google Scholar 

  • Classics Lowry O, Rosebrough N, Farr A et al (1951) Protein measurement with the folin phenol reagent[J]. J Biol Chem 193(1):265–275

    Article  Google Scholar 

  • Cope A, Le Friec G, Cardone J et al (2011) The Th1 life cycle: molecular control of IFN-γ to IL-10 switching[J]. Trends Immunol 32(6):278–286

    Article  PubMed  CAS  Google Scholar 

  • Dawood MAO, Eweedah NM, Elbialy ZI et al (2020) Dietary sodium butyrate ameliorated the blood stress biomarkers, heat shock proteins, and immune response of Nile tilapia (Oreochromis niloticus) exposed to heat stress[J]. J Therm Biol 88:102500

    Article  PubMed  CAS  Google Scholar 

  • Day RD, German DP, Manjakasy JM et al (2011) Enzymatic digestion in stomachless fishes: how a simple gut accommodates both herbivory and carnivory[J]. J Comp Physiol B 181:603–613

    Article  PubMed  CAS  Google Scholar 

  • De Fa L (2019) Research progress of soybean anti-nutritional factors. Feed Animal Husbandry[J] (1):52–58

  • Deng J, Mai K, Ai Q et al (2006) Effects of replacing fish meal with soy protein concentrate on feed intake and growth of juvenile Japanese flounder, Paralichthys olivaceus[J]. Aquaculture 258(1–4):503–513

    Article  CAS  Google Scholar 

  • Fang L, Wang Q, Guo X et al (2021) Effects of dietary sodium butyrate on growth performance, antioxidant capacity, intestinal histomorphology and immune response in juvenile Pengze crucian carp (Carassius auratus Pengze)[J]. Aquac Rep 21:100828

    Article  Google Scholar 

  • Fenglu H, Xiaodan W, Jianlin G et al (2018) Effects of glycinin and β-conglycinin on growth performance and intestinal health in juvenile Chinese mitten crabs ( Eriocheir sinensis )[J]. Fish Shellfish Immunol:84

  • Fuss IJ, Boirivant M, Lacy B et al (2002) The interrelated roles of TGF-β and IL-10 in the regulation of experimental colitis[J]. J Immunol 168(2):900–908

    Article  PubMed  CAS  Google Scholar 

  • Gao S, Chen C, Wang L et al (2013) Histone deacetylases inhibitor sodium butyrate inhibits JAK2/STAT signaling through upregulation of SOCS1 and SOCS3 mediated by HDAC8 inhibition in myeloproliferative neoplasms[J]. Exp Hematol 41(3):261-270.e4

    Article  PubMed  CAS  Google Scholar 

  • Guo W, Liu J, Sun J et al (2020) Butyrate alleviates oxidative stress by regulating NRF2 nuclear accumulation and H3K9/14 acetylation via GPR109A in bovine mammary epithelial cells and mammary glands[J]. Free Radical Biol Med 152:728–742

    Article  CAS  Google Scholar 

  • Horwitz DA, Gray JD, Ohtsuka K et al (1997) The immunoregulatory effects of NK cells: the role of TGF-β and implications for autoimmunity[J]. Immunol Today 18(11):538–542

    Article  PubMed  CAS  Google Scholar 

  • Hu S, Liu H, Qiao S et al (2013) Development of immunoaffinity chromatographic method for isolating glycinin (11S) from soybean proteins[J]. J Agric Food Chem 61(18):4406–4410

    Article  PubMed  CAS  Google Scholar 

  • Jiang L, Wang J, Liu Z et al (2020) Sodium butyrate alleviates lipopolysaccharide-induced inflammatory responses by down-regulation of NF-κB, NLRP3 signaling pathway, and activating histone acetylation in bovine macrophages[J]. Front Vet Sci 7:579674

    Article  PubMed  PubMed Central  Google Scholar 

  • Jinho B, Ali H, Seonghun W et al (2020) Evaluation of seven different functional feed additives in a low fish meal diet for olive flounder, Paralichthys olivaceus[J]. Aquaculture 525(C)

  • Li Fang W, Hong’E L, Huanhuan Y et al (2014) Effects of glycinin on the growth performance, feed utilization and nutritional composition in the young common carp[J]. J South China Agric Univ 35(1):1–6

    Google Scholar 

  • Laura B, Gabriel FB, Paula S et al (2016) Lasting effects of butyrate and low FM/FO diets on growth performance, blood haematology/biochemistry and molecular growth-related markers in gilthead sea bream (Sparus aurata )[J]. Aquaculture 454

  • Li T (2017) Effects of sodium butyrate on intestinal, gill and body health and muscle quality of grass carp and its mechanism Sichuan Agricultural University. 138

  • Li Y, Yang P, Zhang Y et al (2017) Effects of dietary glycinin on the growth performance, digestion, intestinal morphology and bacterial community of juvenile turbot, Scophthalmus maximus L[J]. Aquaculture 479:125–133

    Article  CAS  Google Scholar 

  • Li S, Heng X, Guo L et al (2022) SCFAs improve disease resistance via modulate gut microbiota, enhance immune response and increase antioxidative capacity in the host[J]. Fish Shellfish Immunol 120:560–568

    Article  PubMed  CAS  Google Scholar 

  • Lin S, Luo L (2011) Effects of different levels of soybean meal inclusion in replacement for fish meal on growth, digestive enzymes and transaminase activities in practical diets for juvenile tilapia, Oreochromis niloticus× O. aureus[J]. Animal Feed Sci Technol 168(1–2):80–87

    Article  CAS  Google Scholar 

  • Liu W, Yang Y, Zhang J et al (2014) Effects of dietary microencapsulated sodium butyrate on growth, intestinal mucosal morphology, immune response and adhesive bacteria in juvenile common carp (Cyprinus carpio) pre-fed with or without oxidised oil[J]. Br J Nutr 112(1):15–29

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method[J]. Methods 25(4):402–408

  • Lu MC, Ji JA, Jiang ZY et al (2016) The Keap1–Nrf2–ARE pathway as a potential preventive and therapeutic target: an update[J]. Med Res Rev 36(5):924–963

    Article  PubMed  CAS  Google Scholar 

  • Mallioris P, Kotzamanis Y, Vardali S et al (2022) Modulation of intestinal health and hepatic vacuolation in gilthead sea bream (Sparus aurata) juveniles by a mixture of dietary esterified butyrins, emulsifiers from plants and yeast extracts at low and high fish meal inclusion[J]. Anim Feed Sci Technol 284:115194

    Article  CAS  Google Scholar 

  • Meyer CM, Khan AM, Alcorn JL (2022) Impact of surfactant protein-A on immunomodulatory properties of murine and human breast milk[J]. J Pediatr Gastroenterol Nutr 75(1):97–103

    Article  PubMed  CAS  Google Scholar 

  • Min L, Liang L, Yi DK et al (2020) Effects of glycinin on growth performance, immunity and antioxidant capacity in juvenile golden crucian carp, Cyprinus carpio × Carassius auratus[J]. Aquac Res:51(2)

  • Mokhtar DM, Zaccone G, Alesci A et al (2023) Main components of fish immunity: an overview of the fish immune system[J]. Fishes 8(2):93

    Article  Google Scholar 

  • Ou D, Liu S, Tong C et al (2022) LIM mineralization protein-1 inhibits IL-1β-induced human chondrocytes injury by altering the NF-κB and MAPK/JNK pathways[J]. Exp Ther Med 23(1):1–10

    Google Scholar 

  • Peng S, Defa L, Zheji L et al (2007) Effects of glycinin on IgE-mediated increase of mast cell numbers and histamine release in the small intestine[J]. J Nutr Biochem 19(9)

  • Rosa MM, Amalia EM, Ana S (2005) Antioxidant defenses in fish: biotic and abiotic factors[J]. Rev Fish Biol Fish 15(1–2)

  • Sergio C, Misael R, Camilo P et al (2014) Effects of organic acids on growth performance and digestive enzyme activities of juvenile red drum Sciaenops ocellatus[J]. Aquaculture:433

  • Sies H, Berndt C, Jones DP (2017) Oxidative stress[J]. Annu Rev Biochem 86:715–748

    Article  PubMed  CAS  Google Scholar 

  • Tao L, Gaigai Z, Yue F et al (2019) Dietary soybean antigen impairs growth and health through stress-induced non-specific immune responses in Pacific white shrimp, Litopenaeus vannamei[J]. Fish Shellfish Immunol:84

  • Tian L, Zhou XQ, Jiang WD et al (2017) Sodium butyrate improved intestinal immune function associated with NF-κB and p38MAPK signalling pathways in young grass carp (Ctenopharyngodon idella)[J]. Fish Shellfish Immunol 66:548–563

  • Tu W, Wang H, Li S et al (2019) The anti-inflammatory and anti-oxidant mechanisms of the Keap1/Nrf2/ARE signaling pathway in chronic diseases[J]. Aging Dis 10(3):637

    Article  PubMed  PubMed Central  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M et al (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants[J]. Ecotoxicol Environ Saf 64(2):178–189

    Article  PubMed  CAS  Google Scholar 

  • Wang F, Ma J, Wang KS et al (2015) Blockade of TNF-α-induced NF-κB signaling pathway and anti-cancer therapeutic response of dihydrotanshinone I[J]. Int Immunopharmacol 28(1):764–772

    Article  PubMed  CAS  Google Scholar 

  • Wei-Dan J, Kai H, Jin-Xiu Z et al (2015) Soyabean glycinin depresses intestinal growth and function in juvenile Jian carp (Cyprinus carpio var Jian): protective effects of glutamine[J]. Br J Nutr 114(10)

  • Wing KN, Chik BK (2017) The utilization and mode of action of organic acids in the feeds of cultured aquatic animals[J]. Rev Aquac 9(4)

  • Wu X, Wang L, Xie Q et al (2020) Effects of dietary sodium butyrate on growth, diet conversion, body chemical compositions and distal intestinal health in yellow drum (Nibea albiflora, Richardson)[J]. Aquac Res 51(1):69–79

    Article  CAS  Google Scholar 

  • Xiaoming C, Xueming H, Weixing Z et al (2015) Effects of soybean allergic proteins on growth, digestion and non-specific immune of Litopenaeus vannamei[J]. Chin J Anim Nutr 27(07):2115–2127

  • Xu H, Ren M, Liang H et al (2022) Interactive effects of water salinity and dietary methionine levels on growth performance, whole-body composition, plasma parameters, and expression of major nutrient metabolism genes in juvenile genetically improved farmed Tilapia (Oreochromis niloticus)[J]. Aquaculture 546:737381

    Article  CAS  Google Scholar 

  • Xudong S, Shengbin L, Chunhui J et al (2020) Sodium butyrate reduces bovine mammary epithelial cell inflammatory responses induced by exogenous lipopolysaccharide, by inactivating NF-κB signaling[J]. J Dairy Sci 103(9)

  • Ya-lin Z, Xu-Dong D, Lin F et al (2020) Soybean glycinin impaired immune function and caused inflammation associated with PKC-ζ/NF-κb and mTORC1 signaling in the intestine of juvenile grass carp (Ctenopharyngodon idella )[J]. Fish Shellfish Immunol:106

  • Yang L, Zhichu C, Jihong D et al (2019) Sodium butyrate supplementation in high-soybean meal diets for turbot ( Scophthalmus maximus L.): effects on inflammatory status, mucosal barriers and microbiota in the intestine[J]. Fish Shellfish Immunol:88

  • Yanxian L, Pei Y, Yanjiao Z et al (2017) Effects of dietary glycinin on the growth performance, digestion, intestinal morphology and bacterial community of juvenile turbot, Scophthalmus maximus L[J]. Aquaculture:479

  • Yin B, Liu H, Tan B et al (2021) MHC II-PI3K/Akt/mTOR signaling pathway regulates intestinal immune response induced by soy glycinin in hybrid grouper: protective effects of sodium butyrate[J]. Front Immunol 11:615980

    Article  PubMed  PubMed Central  Google Scholar 

  • Youling G, Trond S, Karl DS et al (2011) Supplementation of fishmeal and plant protein-based diets for rainbow trout with a mixture of sodium formate and butyrate[J]. Aquaculture 311(1–4)

  • Zapata A, Diez B, Cejalvo T et al (2006) Ontogeny of the immune system of fish[J]. Fish Shellfish Immunol 20(2):126–136

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Duan X, Feng L et al (2020a) Soybean glycinin impaired immune function and caused inflammation associated with PKC-ζ/NF-κb and mTORC1 signaling in the intestine of juvenile grass carp (Ctenopharyngodon idella)[J]. Fish ShellfishImmunol 106:393–403

  • Zhang Y, Jiang WD, Duan X et al (2020b) Soybean glycinin caused NADPH-oxidase-regulated ROS overproduction and decreased ROS elimination capacity in the mid and distal intestine of juvenile grass carp (Ctenopharyngodon idella)[J]. Aquaculture 516:734651

  • Zhu D (2008) Study on the distribution of soybean allergenic proteins in carpintestinal tissue Jilin Agricultural University. 65

  • Zhu R, Li L, Li M et al (2021) Effects of dietary glycinin on the growth performance, immunity, hepatopancreas and intestinal health of juvenile Rhynchocypris lagowskii Dybowski[J]. Aquaculture 544:737030

    Article  CAS  Google Scholar 

Download references

Funding

Jilin Science and Technology Innovation and Entrepreneurship Excellence for Young and Middle-aged People (Team) Project (Innovation Category), No. 20230508008RC.

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Authors and Affiliations

  1. College of Animal Science and Technology, Jilin Agriculture University, Changchun, 130118, China

    Deng-Lai Li, Si-Ying Liu, Rui Zhu, Si-Tong Meng, Yin-Tao Wang, Zhi-Yong Yang, Liang Li, Xiao-Fang Wei, Guo-Jun Shang, Hao-Tong Wang & Li-Fang Wu

  2. Key Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, 130118, China

    Deng-Lai Li, Si-Ying Liu, Rui Zhu, Si-Tong Meng, Yin-Tao Wang, Zhi-Yong Yang, Liang Li, Xiao-Fang Wei, Guo-Jun Shang, Hao-Tong Wang & Li-Fang Wu

  3. Jilin Provincial Key Laboratory of Animal Nutrition and Feed Science, Jilin Agricultural University, Changchun, 130118, China

    Deng-Lai Li, Si-Ying Liu & Li-Fang Wu

  4. Institute of Animal Nutrition and Feed, Jilin Academy of Agricultural Sciences, Jilin, China

    Zi-Hui Qu

  5. Jingyuetan Reservoir Management Office, Changchun, 130118, China

    Ya-Nan Quan

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  1. Deng-Lai Li
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Contributions

Deng-Lai Li carried out the experiments, analyzed the data, and wrote the manuscript. Si-Ying Liu, Rui Zhu, Si-Tong Meng, Yin-Tao Wang, Zhi-Yong Yang, Liang Li, Guo-Jun Shang, Xiao-Fang Wei, Hao-Tong Wang, Zi-Hui Qu, and Ya-Nan Quan sampled and contributed reagents/materials. Li-Fang Wu conceived the study and designed the experiments. All authors read and approved the final manuscript. All authors read and approved the final manuscript.

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Correspondence to Li-Fang Wu.

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This study was using only laboratory animals that were handled according to approval by the Institutional Animal Care and Use Committee of Jilin Agricultural University (approval number: 20220923004).

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Li, DL., Liu, SY., Zhu, R. et al. Potential protective effects of sodium butyrate on glycinin-induced oxidative stress, inflammatory response, and growth inhibition in Cyprinus carpio. Fish Physiol Biochem 50, 273–293 (2024). https://doi.org/10.1007/s10695-023-01276-4

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