Abstract
The study investigated the alleviated effects of Alpha-ketoglutaric acid (AKG) on the intestinal health of mirror carp (Cyprinus carpio Songpu) caused by soy antigenic protein. The diets were formulated from fishmeal (CON), 50% soybean meal (SBM), the mixture of glycinin and β-conglycinin (11 + 7S) and adding 1% AKG in the 11 + 7S (AKG). Carp (~ 4 g) in triplicate (30 fish per tank) was fed to apparent satiation thrice a day for six weeks. Compared with CON, SBM treatment resulted in significantly poor growth performance (P < 0.05), whereas 11 + 7S and AKG treatments were not significantly different from CON (P > 0.05). Gene expression of tumor necrosis factor (TNF-α) and interleukin-1 β (IL-1β) in proximal intestines (PI) and distal intestines (DI) were increased (P < 0.05), and transforming growth factor (TGF-β) in PI and middle intestines (MI) was decreased (P < 0.05) in both SBM and 11 + 7S. The caspase-3 in DI increased in SBM (P < 0.05) and the caspase-3 and caspase-9 in DI increased in 11 + 7S (P < 0.05); conversely, TGF-β in PI and MI was increased, TNF-α and IL-1β in the MI, caspase-3, and caspase-9 in DI was decreased in AKG (P < 0.05). The TOR (target of rapamycin) in PI and MI, ACC in PI, MI and DI was decreased in SBM (P < 0.05), the AMPK in the PI and DI, TOR in PI, MI and DI, ACC in PI and DI, 4E-BP in DI was reduced in 11 + 7S (P < 0.05). AMPK in the PI and DI, ACC in the PI and MI, TOR in PI, MI, and DI, 4E-BP in PI and DI was recovered by AKG supplementation (P < 0.05). Lipids and lipid-like metabolism, organic acids and derivatives metabolism increased in AKG dietary treatment. In conclusion, AKG reduces the expression of intestinal inflammation and apoptosis pathway and changes glycerophospholipid metabolism and sphingolipid metabolism in the intestine of fish.
Similar content being viewed by others
Data availability
The datasets used or analysed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
Abbreviations
- AKG:
-
Alpha-ketoglutaric acid
- TNF-α,:
-
Tumor necrosis factor
- IL-1β:
-
Interleukin-1 β
- TGF-β:
-
Transforming growth factor
- WG:
-
Weight gain
- FCR:
-
Feed conversion ratio
- CF:
-
Condition factor
- SR:
-
Survival rate
- PER:
-
Protein efficiency ratio
- SGR:
-
Specific growth rate
- PI:
-
Proximal intestines
- MI:
-
Middle intestines
- DI:
-
Distal intestines
References
Abu-Elheiga L, Jayakumar A, Baldini A, Chirala SS, Wakil SJ (1995) Human acetyl-coa carboxylase: characterization, molecular cloning, and evidence for two isoforms. Proc Natl Acad Sci 92(9):4011–4015. https://doi.org/10.1073/pnas.92.9.4011
Ai F, Wang LS, Li JN, Xu QY (2019) Effects of a-ketoglutarate (AKG) supplementation in low phosphorous dietson the growth, phosphorus metabolism and skeletal development of juvenilemirror carp (Cyprinus carpio). Aquaculture 07:393–401. https://doi.org/10.1016/j.aquaculture.03.047
Azar R, Alard A, Susini C, Bousquet C, Pyronnet S (2006) 4e-bp1 is a target of smad4 essential for tgfβ-mediated inhibition of cell proliferation. Urologe 45(10):1266–1270. https://doi.org/10.1038/emboj.2009.291
Barnes BR, Marklund S, Steiler TL, Walter M, Andersson L (2004) The 5′-amp-activated protein kinase γ3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle. J Biol Chem 279(37):38441–38447. https://doi.org/10.1074/jbc.M405533200
Boutin JA, Meunier F, Lambert PH, Hennig P, Volland JP (1993) In vivo and in vitro glucuronidation of the flavonoid diosmetin in rats. Drug Metab Disp 21(6):1157–1166. https://doi.org/10.1002/ddr.430300311
Buttke TM, Sandstrom PA (1994) Oxidative stress as a mediator of apoptosis. Immunol Today 15:7–10. https://doi.org/10.1016/0167-5699(94)90018-3
Chasiotis H, Kelly SP (2011) Effect of cortisol on permeability and tight junction protein transcript abundance in primary cultured gill epithelia from stenohaline goldfish and euryhaline trout. Gen Comp Endocrinol 172(3):494–504. https://doi.org/10.1016/j.ygcen.2011.04.023
Chasiotis H, Kolosov D, Kelly SP (2012) Permeability properties of the teleost gill epithelium under ion-poor conditions. Am J Physiol Regul Integr Comp Physiol 302(6):R727–R739. https://doi.org/10.1152/ajpregu.00577.2011
Duan XD, Feng L, Jiang WD, Pei Wu, Yang L, Kuang SY, Tang WN, Zhang YN, Zhou XQ (2019) Dietary soybean β-conglycinin suppresses growth performance and inconsistently triggers apoptosis in the intestine of juvenile grass carp (Ctenopharyngodon idella) in association with ROS-mediated MAPK signalling. Aquac Nutr 25:770–782. https://doi.org/10.1111/anu.12895
Fast MD, Johnson SC, Johns S (2007) Differential expression of the pro-inflammatory cytokines IL-1b-1, TNFa-1 and IL-8 in vaccinated pink (oncorhynchus gorbuscha) and chum (oncorhynchus keta) salmon juveniles. Fish Shellfish Immunol 22(4):403–407. https://doi.org/10.1016/j.fsi.2006.06.012
Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147:742–758. https://doi.org/10.1016/j.cell.2011.11.045
Guo SS, Duan R, Wang L, Hou YQ, Tan LL, Cheng Q, Liao M, Ding BY (2017) Dietary a-ketoglutarate supplementation improves hepatic and intestinal energy status and anti-oxidative capacity of Cherry Valley ducks. Anim Sci J 88:1753–1762. https://doi.org/10.1111/asj.12824
Han FL, Wang XD, Guo CL, Xu CQ (2018) Effects of glycinin and β-conglycinin on growth performance and intestinal health in juvenile Chinese mitten crabs (Eriocheir sinensis). Fish Shellfish Immunol 84:269–279. https://doi.org/10.1016/j.fsi.2018.10.013
Hardie DG, Sakamoto K (2006) AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology 21(1):48–60. https://doi.org/10.1152/physiol.00044.2005
Hayashi T, Hirshman MF, Fujii N, Habinowski SA, Witters LA, Goodyear LJ (2000) Metabolic stress and altered glucose transport: activation of amp-activated protein kinase as a unifying coupling mechanism. Diabetes 49(4):527–531. https://doi.org/10.2337/diabetes.49.4.527
Hossain S, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Islam J (2018) Substitution of dietary fishmeal by soybean meal with inosine administration influences growth, digestibility, immunity, stress resistance and gut morphology of juvenile amberjack seriola dumerili. Aquaculture 488:174–188. https://doi.org/10.1016/j.aquaculture.2018.01.037
Iwashita Y, Suzuki N, Matsunari H, Sugita T, Yamamoto T (2009) Influence of soya saponin, soya lectin, and cholyltaurine supplemented to a casein-based semipurified diet on intestinal morphology and biliary bile status in fingerling rainbow trout oncorhynchus mykiss. Fish Sci 75(5):1307–1315. https://doi.org/10.1007/s12562-009-0158-1
Jiang WD, Hu K, Zhang JX, Liu Y, Jiang J, Wu P (2015) Soyabean glycinin depresses intestinal growth and function in juvenile jian carp (cyprinus carpio var jian): protective effects of glutamine. Br J Nutr 114:1569–1583. https://doi.org/10.1017/S0007114515003219
Kortner TM, Skugor S, Penn MH, Mydland LT, Djordjevic B, Hillestad M, Krasnov A, Krogdhl A (2012) Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar). BioMed Central 8:101. https://doi.org/10.1186/1746-6148-8-101
Krause G, Winkler L, Piehl C, Blasig I, Piontek J, Piontek J, Mueller SL (2010) Structure and Function of Extracellular Claudin Domains. Ann N Y Acad Sci 1165:34–43. https://doi.org/10.1111/j.1749-6632.2009.04057.x
Krogdahl A, Bakke‐McKellep A M, Baeverfjord G (2015) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (salmo salar L.). Aquac Nutr 9(6):361–371. https://doi.org/10.1046/j.1365-2095.2003.00264.x
Li Y, Hu H, Liu J, Yang P, Zhang Y, Ai Q (2017a) Dietary soya allergen β-conglycinin induces intestinal inflammatory reactions, serum-specific antibody response and growth reduction in a carnivorous fish species, turbot scophthalmus maximus l. Aquac Res. https://doi.org/10.1111/are.13224
Li Y, Yang P, Zhang Y, Ai Q, Xu W, Zhang W (2017b) Effects of dietary glycinin on the growth performance, digestion, intestinal morphology and bacterial community of juvenile turbot, scophthalmus maximus l. Aquaculture 479:125–133. https://doi.org/10.1016/j.aquaculture.2017.05.008
Lin SM, Li 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. Animal Feed Comparison Science and Technology 168:80–87. https://doi.org/10.1016/j.anifeedsci.2011.03.012
Luo QH, Zhou ZL, Zhao JH, Xu H, Limbu SM, Xu QY (2023) Dietary β-conglycinin induces intestinal enteritis and affects glycerophospholipid and arginine metabolism in mirror carp (Cyprinus carpio). Aquaculture 567:739257. https://doi.org/10.1016/j.aquaculture.2023.739257
Luo QH, Qian RD, Qiu ZS, Yamamoto FY, Du YY, Lin XW, Zhao JH, Xu QY (2023b) Dietary a-ketoglutarate alleviates glycinin and b-conglycinin induced damage in the intestine of mirror carp (Cyprinus carpio). Front Immunol 14:1140012. https://doi.org/10.3389/fimmu.2023.1140012
Lygren B, Hamre K, Waagb R (2001) Effect of induced hyperoxia on the antioxidant status of atlantic salmon salmo salar l. fed three different levels of dietary vitamin E. Aquac Res 31:401–407. https://doi.org/10.1046/j.1365-2109.2000.00459.x
Mazdak BL, Wright SI, Kelly SP (2008) Claudin-3 tight junction proteins in Tetraodon nigroviridis: cloning, tissue-specific expression, and a role in hydromineral balance. Am J Physiol Regul Integr Comp Physiol 294(5):R1638-47. https://doi.org/10.1152/ajpregu.00039.2008
NRC (2011) Nutrient Requirements of Fish and Shrimp. National Academy Press, Washington, DC
Sahlmann C, Sutherland B, Kortner TM, Koop BF, Krogdahl A, Bakke AM (2013) Early response of gene expression in the distal intestine of atlantic salmon (salmo salar L.) during the development of soybean meal induced enteritis. Fish Shellfish Immunol 34:599–609. https://doi.org/10.1016/j.fsi.2012.11.031
Santigosa E, Miguel R, Rodiles A, Barroso FG, Alarcón FJ (2010) Effect of diets containing a purified soybean trypsin inhibitor on growth performance, digestive proteases and intestinal histology in juvenile sea bream (sparus aurata L.). Aquac Res 41:e187–e198. https://doi.org/10.1111/j.1365-2109.2010.02500.x
Sharifi AM, Eslami H, Larijani B, Davood J (2009) Involvement of caspase-8, -9, and -3 in high glucose-induced apoptosis in PC12 cells. Neurosci Lett 459(2):47–51. https://doi.org/10.1016/j.neulet.2009.03.100
Sperstad S, Bakke-Mckellep AM, Penn MH, Salas PM, Krogdahl Å (2007) Effects of dietary soybean meal, inulin and oxytetracycline on gastrointestinal histological characteristics, distal intestine cell proliferation and intestinal microbiota in Atlantic salmon (Salmo salar L.). Br J Nutr 97(4):699–713. https://doi.org/10.1017/S0007114507381397
Tain LS, Mortiboys H, Tao RN, Ziviani E, Bandmann O, Whitworth AJ (2009) Rapamycin activation of 4e-bp prevents parkinsonian dopaminergic neuron loss. Nat Neurosci 12:1129–1135. https://doi.org/10.1038/nn.2372
Urán PA, Gonalves AA, Taverne-Thiele JJ, Schrama JW, Rombout J (2009) Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 25:751–760. https://doi.org/10.1016/j.fsi.2008.02.013
Wang X, Sun H, Zhang A, Ping W, Han Y (2011) Ultra-performance liquid chromatography coupled to mass spectrometry as a sensitive and powerful technology for metabolomic studies. J Sep Sci 34(24):3451–3459. https://doi.org/10.1002/jssc.201100333
Wei Y, Liang M, Mai K, Zheng K, Xu H (2017) 1H NMR-based metabolomics studies on the effect of size-fractionated fish protein hydrolysate, fish meal and plant protein in diet for juvenile turbot (Scophthalmus maximus L). Aquac Nutr 23(3):523–536. https://doi.org/10.1111/anu.12420
Wilson S, Blaschek K, Mejia EG (2005) Allergenic Proteins in Soybean: Processing and Reduction of P34 Allergenicity. Nutr Rev 63(2):47–58. https://doi.org/10.1111/j.1753-4887.2005.tb00121.x
Wu D, Fan Z, Li J, Zhang Y, Xu Q, Wang L, Wang L (2022) Low Protein Diets Supplemented With Alpha-Ketoglutarate Enhance the Growth Performance, Immune Response, and Intestinal Health in Common Carp (Cyprinus carpio). Front Immunol 13:915657. https://doi.org/10.3389/fimmu.2022.915657
Yadav G, Meena DK, Sahoo AK, Das BK, Sen R (2020) Effective valorization of microalgal biomass for the production of nutritional fish-feed supplements. J Clean Prod 243:118697. https://doi.org/10.1016/j.jclepro.2019.118697
Zhang JX, Guo LY, Lin F, Jiang WD, Kuang SY, Liu Y (2014) Soybean β-conglycinin induces inflammation and oxidation and causes dysfunction of intestinal digestion and absorption in fish. Plos One 8(3):e58115. https://doi.org/10.1371/journal.pone.0058115
Zhang C, Rahimnejad S, Wang YR, Lu K, Kai S, Ling W (2018) Substituting fish meal with soybean meal in diets for japanese seabass (Lateolabrax japonicus): effects on growth, digestive enzymes activity, gut histology, and expression of gut inflammatory and transporter genes. Aquaculture 483:173–182. https://doi.org/10.1016/j.aquaculture.2017.10.029
Zhao JY, Xu QY (2022) Influence of soybean meal on intestinal mucosa metabolome and effects of adenosine monophosphate-activated protein kinase signaling pathway in mirror carp (Cyprinus carpio Songpu). Front Mar Sci 9:844716. https://doi.org/10.3389/fmars.2022.844716
Zhao Y, Qin G, Han R, Wang J, Zhang X, Liu D (2014) β-conglycinin reduces the tight junction occludin and zo-1 expression in ipec-j2. Int J Mol Sci 15:1915–1926. https://doi.org/10.3390/ijms15021915
Zhao Y, Liu D, Zhang S, Pan L, Qin G (2017) Different Damage to the Mechanical Barrier Function of IPEC-J2 Induced by Soybean Allergen β-conglycinin Hydrolyzed Peptides. Int J Food Eng 13(10):2–7. https://doi.org/10.1515/ijfe-2016-0370
Zhao JH, Yang X, Qiu ZS, Zhang RF, Xu H, Wang T (2023) Effects of tributyrin and alanyl-glutamine dipeptide on intestinal health of largemouth bass (Micropterus salmoides) fed with high soybean meal diet. Front Immunol 14:1140678. https://doi.org/10.3389/fimmu.2023.1140678
Acknowledgements
The funding support provided by the Natural Science Foundation of China, NSFC (31972800) and Key Laboratory of Freshwater Aquatic Biotechnology and Genetic Breeding of Ministry of Agriculture Key Laboratory (HSY202209K1) is gratefully acknowledged. The authors are grateful to the Dr. Zhili Ding for providing necessary facilities and support to successfully carry out this study.
Funding
Funded by the Natural Science Foundation of China, NSFC (31972800), Key Laboratory of Freshwater Aquatic Biotechnology and Genetic Breeding of Ministry of Agriculture Key Laboratory (HSY202209K1).
Author information
Authors and Affiliations
Contributions
Zuliang Zhou have participated in conceptualization, methodology, data statistics and writing—Original Draft conception; Jianhua Zhao participated in conceptualization, methodology; Clement R. de Cruz completed writing—review & editing; Hong Xu and Liansheng Wang analyzed; Qiyou Xu participated in conceptualization, writing—review & editing and supervision.
Corresponding author
Ethics declarations
Ethical Approval
The study was conducted strictly following the Guidance of the Care and Use of Laboratory Animals in China. The experimental protocol was approved by the Committee on the Ethics of Animal Experiments of Huzhou University (20180306).
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhou, Z., Zhao, J., de Cruz, C.R. et al. Alpha-ketoglutaric acid mitigates the detrimental effects of soy antigenic protein on the intestinal health and growth performance of Mirror carp Cyprinus carpio. Fish Physiol Biochem 49, 951–965 (2023). https://doi.org/10.1007/s10695-023-01234-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-023-01234-0