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Soyabean glycinin depresses intestinal growth and function in juvenile Jian carp (Cyprinus carpio var Jian): protective effects of glutamine

  • Wei-Dan Jiang (a1) (a2) (a3), Kai Hu (a1) (a4), Jin-Xiu Zhang (a1), Yang Liu (a1) (a2) (a3), Jun Jiang (a1), Pei Wu (a1) (a2) (a3), Juan Zhao (a1), Sheng-Yao Kuang (a5), Ling Tang (a5), Wu-Neng Tang (a5), Yong-An Zhang (a6), Xiao-Qiu Zhou (a1) (a2) (a3) and Lin Feng (a1) (a2) (a3)...


This study investigated the effects of glycinin on the growth, intestinal oxidative status, tight junction components, cytokines and apoptosis signalling factors of fish. The results showed that an 80 g/kg diet of glycinin exposure for 42 d caused poor growth performance and depressed intestinal growth and function of juvenile Jian carp (Cyprinus carpio var. Jian). Meanwhile, dietary glycinin exposure induced increases in lipid peroxidation and protein oxidation; it caused reductions in superoxide dismutase (SOD), catalase and glutathione peroxidase (GPx) activities; and it increased MnSOD, CuZnSOD, GPx1b and GPx4a mRNA levels, suggesting an adaptive mechanism against stress in the intestines of fish. However, dietary glycinin exposure decreased both the activity and mRNA levels of nine isoforms of glutathione-S-transferase (GST) (α, μ, π, ρ, θ, κ, mGST1, mGST2 and mGST3), indicating toxicity to this enzyme activity and corresponding isoform gene expressions. In addition, glycinin exposure caused partial disruption of intestinal cell–cell tight junction components, disturbances of cytokines and induced apoptosis signalling in the distal intestines>mid intestines>proximal intestines of fish. Glycinin exposure also disturbed the mRNA levels of intestinal-related signalling factors Nrf2, Keap1a, Keap1b, eleven isoforms of protein kinase C and target of rapamycin/4E-BP. Interestingly, glutamine was observed to partially block those negative influences. In conclusion, this study indicates that dietary glycinin exposure causes intestinal oxidative damage and disruption of intestinal physical barriers and functions and reduces fish growth, but glutamine can reverse those negative effects in fish. This study provides some information on the mechanism of glycinin-induced negative effects.

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Corresponding author

* Corresponding authors: X.-Q. Zhou, fax +86 835 288 5968, email; L. Feng,


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These three authors contributed equally to this work.



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1. Brinker, A & Friedrich, C (2012) Fish meal replacement by plant protein substitution and guar gum addition in trout feed. Part II: Effects on faeces stability and rheology. Biorheology 49, 2748.
2. Silva-Carrillo, Y, Hernández, C, Hardy, RW, et al. (2012) The effect of substituting fish meal with soybean meal on growth, feed efficiency, body composition and blood chemistry in juvenile spotted rose snapper Lutjanus guttatus (Steindachner, 1869). Aquaculture 364, 180185.
3. Zhao, Y, Qin, G, Sun, Z, et al. (2011) Effects of soybean agglutinin on intestinal barrier permeability and tight junction protein expression in weaned piglets. Int J Mol Sci 12, 85028512.
4. Wang, T, Qin, G, Sun, Z, et al. (2014) Advances of research on glycinin and β-conglycinin: a review of two major soybean allergenic proteins. Crit Rev Food Sci 54, 850862.
5. Zhao, Y, Qin, GX, Sun, ZW, et al. (2010) Effects of glycinin and β-conglycinin on enterocyte apoptosis, proliferation and migration of piglets. Food Agr Immunol 21, 209218.
6. Jiang, WD, Wu, P, Kuang, SY, et al. (2011) Myo-inositol prevents copper-induced oxidative damage and changes in antioxidant capacity in various organs and the enterocytes of juvenile Jian carp (Cyprinus carpio var. Jian). Aquat Toxicol 105, 543551.
7. Jiang, WD, Feng, L, Liu, Y, et al. (2009) Growth, digestive capacity and intestinal microflora of juvenile Jian carp (Cyprinus carpio var. Jian) fed graded levels of dietary inositol. Aquac Res 40, 955962.
8. Wen, HL, Feng, L, Jiang, WD, et al. (2014) Dietary tryptophan modulates intestinal immune response, barrier function, antioxidant status and gene expression of TOR and Nrf2 in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immun 40, 275287.
9. Chen, J, Zhou, XQ, Feng, L, et al. (2009) Effects of glutamine on hydrogen peroxide-induced oxidative damage in intestinal epithelial cells of Jian carp (Cyprinus carpio var. Jian). Aquaculture 288, 285289.
10. Xu, J, Zhou, A, Wang, Z, et al. (2010) Effects of glycinin and β-conglycinin on integrity and immune responses of mouse intestinal epithelial cells. J Anim Plant Sci 20, 170174.
11. Turan, A & Mahmood, A (2007) The profile of antioxidant systems and lipid peroxidation across the crypt-villus axis in rat intestine. Digest Dis Sci 52, 18401844.
12. Kohen, R & Nyska, A (2002) Invited review: oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30, 620650.
13. Jiang, WD, Liu, Y, Jiang, J, et al. (2015) Copper exposure induces toxicity to the antioxidant system via the destruction of Nrf2/ARE signaling and caspase-3-regulated DNA damage in fish muscle: amelioration by myo-inositol. Aquat Toxicol 159, 245255.
14. Kobayashi, A, Kang, M, Watai, Y, et al. (2006) Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol Cell Biol 26, 221229.
15. Zhao, Y, Liu, D, Han, R, et al. (2015) Soybean allergen glycinin induced the destruction of the mechanical barrier function in IPEC-J2. Food Agr Immunol 26, 601609.
16. Unger, RE, Krump-Konvalinkova, V, Peters, K, et al. (2002) In vitro expression of the endothelial phenotype: Comparative study of primary isolated cells and cell lines, including the novel cell line HPMEC-ST1. 6R. Microvasc Res 64, 384397.
17. Loh, YH, Christoffels, A, Brenner, S, et al. (2004) Extensive expansion of the claudin gene family in the teleost fish, Fugu rubripes. Genome Res 14, 12481257.
18. Capaldo, CT & Nusrat, A (2009) Cytokine regulation of tight junctions. Biochim Biophys Acta 1788, 864871.
19. Feng, K, Zhang, G, Wei, K, et al. (2012) Molecular characterization of cholecystokinin in grass carp (Ctenopharyngodon idellus): cloning, localization, developmental profile, and effect of fasting and refeeding on expression in the brain and intestine. Fish Physiol Biochem 38, 18251834.
20. Hoyle, I, Shaw, BJ & Handy, RD (2007) Dietary copper exposure in the African walking catfish, Clarias gariepinus: transient osmoregulatory disturbances and oxidative stress. Aquat Toxicol 83, 6272.
21. Zeng, Z, Wang, R, Shi, Y, et al. (2014) MLN0128, a second-generation mTOR kinase inhibitor, disrupts survival signaling and triggers apoptosis in AML. Blood 124, 3613.
22. Satoh, J, Tsujikawa, T, Fujiyama, Y, et al. (2003) Nutritional benefits of enteral alanyl–glutamine supplementation on rat small intestinal damage induced by cyclophosphamide. J Gastroen Hepatol 18, 719725.
23. Lin, Y & Zhou, XQ (2006) Dietary glutamine supplementation improves structure and function of intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture 256, 389394.
24. Zhang, JX, Guo, LY, Feng, L, et al. (2013) Soybean β-conglycinin induces inflammation and oxidation and causes dysfunction of intestinal digestion and absorption in fish. PLOS ONE 8, e58115.
25. Utsumi, S, Matsumura, Y & Mori, T (1997) Structure–function relationships of soy proteins. In Food Protein and their Applications, pp. 257292 [S Damodaran and A Paraf, editors]. New York: Marcel Dekker.
26. Zhang, JX, Zhou, XQ & Liu, Y (2007) Effects of soybean meal on the growth and intestinal immunity of juvenile Jian carp. Aquacult Sci 2, 315320.
27. Sun, P, Li, D, Li, Z, et al. (2008) Effects of glycinin on IgE-mediated increase of mast cell numbers and histamine release in the small intestine. J Nutr Biochem 19, 627633.
28. Jiang, TT, Feng, L, Liu, Y, et al. (2014) Effects of exogenous xylanase supplementation in plant protein-enriched diets on growth performance, intestinal enzyme activities and microflora of juvenile Jian carp (Cyprinus carpio var. Jian). Aquacult Nutr 20, 632645.
29. Jiang, WD, Liu, Y, Hu, K, et al. (2014) Copper exposure induces oxidative injury, disturbs the antioxidant system and changes the Nrf2/ARE (CuZnSOD) signaling in the fish brain: protective effects of myo-inositol. Aquat Toxicol 155, 301313.
30. Xiao, WW, Feng, L, Liu, Y, et al. (2011) Effects of dietary methionine hydroxy analogue supplement on growth, protein deposition and intestinal enzymes activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquacult Nutr 17, 408417.
31. Bohne, VJB, Hamre, K & Arukwe, A (2007) Hepatic metabolism, phase I and II biotransformation enzymes in Atlantic salmon (Salmo Salar, L) during a 12 week feeding period with graded levels of the synthetic antioxidant, ethoxyquin. Food Chem Toxicol 45, 733746.
32. Qu, RJ, Wang, XH, Feng, MB, et al. (2013) The toxicity of cadmium to three aquatic organisms (Photobacterium phosphoreum, Daphnia magna and Carassius auratus) under different pH levels. Ecotox Environ Safe 95, 8390.
33. Bessey, OA, Lowry, OH & Brook, MJ (1964) Rapid colouring method for determination of alkaline phosphatase in five cubic millimeters of serum. J Biol Chem 164, 321329.
34. Weng, CF, Chiang, CC, Gong, HY, et al. (2002) Acute changes in gill Na+-K+-ATPase and creatine kinase in response to salinity changes in the euryhaline teleost, tilapia (Oreochromis mossambicu . Physiol Biochem Zool 75, 2936.
35. Bauermeister, A, Lewendon, A, Ramage, P, et al. (1983) Distribution and some properties of the glutathione S-transferase and γ-glutamyl transpeptidase activities of rainbow trout. Comp Biochem Phys C 74, 8993.
36. Tanzer, ML & Gilvarg, C (1959) Creatine and creatine kinase measurement. J Biol Chem 234, 32013204.
37. Gornicka, A, Fettig, J, Eguchi, A, et al. (2012) Adipocyte hypertrophy is associated with lysosomal permeability both in vivo and in vitro: role in adipose tissue inflammation. Am J Physiol Endoc Metab 303, E597E606.
38. Xu, S, Zhou, Z, Zhang, L, et al. (2010) Exposure to 1800 MHz radiofrequency radiation induces oxidative damage to mitochondrial DNA in primary cultured neurons. Brain Res 1311, 189196.
39. Baltacıoğlu, E, Akalın, FA, Alver, A, et al. (2008) Protein carbonyl levels in serum and gingival crevicular fluid in patients with chronic periodontitis. Arch Oral Biol 53, 716722.
40. Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248254.
41. Zhang, X, Zhu, Y, Cai, L, et al. (2008) Effects of fasting on the meat quality and antioxidant defenses of market-size farmed large yellow croaker (Pseudosciaena crocea). Aquaculture 280, 136139.
42. Jiang, W, Feng, L, Liu, Y, et al. (2009) Myo-inositol prevents oxidative damage, inhibits oxygen radical generation and increases antioxidant enzyme activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Res 40, 17701776.
43. Lushchak, VI, Lushchak, LP, Mota, AA, et al. (2001) Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. Am J Physiol Regul Integr Comp Physiol 280, R100R107.
44. Vardi, N, Parlakpinar, H, Ozturk, F, et al. (2008) Potent protective effect of apricot and β-carotene on methotrexate-induced intestinal oxidative damage in rats. Food Chem Toxicol 46, 30153022.
45. Datkhile, KD, Mukhopadhyaya, R, Dongre, TK, et al. (2009) Increased level of superoxide dismutase (SOD) activity in larvae of Chironomus ramosus (Diptera: Chironomidae) subjected to ionizing radiation. Comp Biochem Physiol C Toxicol Pharmacol 149, 500506.
46. Wang, L & Gallagher, EP (2013) Role of Nrf2 antioxidant defense in mitigating cadmium-induced oxidative stress in the olfactory system of zebrafish. Toxicol Appl Pharm 266, 177186.
47. Collins, SA, Desai, AR, Mansfield, GS, et al. (2012) The effect of increasing inclusion rates of soybean, pea and canola meals and their protein concentrates on the growth of rainbow trout: Concepts in diet formulation and experimental design for ingredient evaluation. Aquaculture 344–349, 9099.
48. Holzhauser, T, Wackermann, O, Ballmer-Weber, BK, et al. (2009) Soybean (Glycine max) allergy in Europe: Gly m 5 (β-conglycinin) and Gly m 6 (glycinin) are potential diagnostic markers for severe allergic reactions to soy. J Allergy Clin Immun 123, 452458.
49. Chen, GF, Feng, L, Kuang, SY, et al. (2012) Effect of dietary arginine on growth, intestinal enzyme activities and gene expression in muscle, hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Brit J Nutr 108, 195207.
50. Ma, X, He, P, Sun, P, et al. (2010) Lipoic acid: an immunomodulator that attenuates glycinin-induced anaphylactic reactions in a rat model. J Agr Food Chem 58, 50865092.
51. Gu, M, Bai, N, Xu, W, et al. (2014) Effects of dietary β-conglycinin and glycinin on digestive enzymes activities, intestinal histology and immune responses of juvenile turbot Scophthalmus maximus . Aquac Res (epublication ahead of print version 16 August 2014).
52. Liang, Q, Sheng, Y, Jiang, P, et al. (2011) The gender-dependent difference of liver GSH antioxidant system in mice and its influence on isoline-induced liver injury. Toxicology 280, 6169.
53. Moellering, D, Mc Andrew, J, Patel, RP, et al. (1999) The induction of GSH synthesis by nanomolar concentrations of NO in endothelial cells: a role for γ-glutamylcysteine synthetase and γ-glutamyl transpeptidase. Febs Lett 448, 292296.
54. Fontagné-Dicharry, S, Lataillade, E, Surget, A, et al. (2014) Antioxidant defense system is altered by dietary oxidized lipid in first-feeding rainbow trout (Oncorhynchus mykiss). Aquaculture 424, 220227.
55. Ferro, D, Franchi, N, Mangano, V, et al. (2013) Characterization and metal-induced gene transcription of two new copper zinc superoxide dismutases in the solitary ascidian Ciona intestinalis . Aquat Toxicol 140, 369379.
56. Nebert, DW & Vasiliou, V (2004) Analysis of the glutathione S-transferase (GST) gene family. Hum Genomics 1, 460464.
57. Uno, Y, Murayama, N, Kunori, M, et al. (2013) Characterization of microsomal glutathione S-transferases MGST1, MGST2, and MGST3 in Cynomolgus macaque . Drug Metab Dispos 41, 16211625.
58. He, S, Liang, X, Sun, J, et al. (2013) Induction of liver GST transcriptions by tert-butylhydroquinone reduced microcystin-LR accumulation in Nile tilapia (Oreochromis niloticus). Ecotox Environ Safe 90, 128135.
59. Itoh, K, Wakabayashi, N, Katoh, Y, et al. (2003) Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8, 379391.
60. Niture, SK, Jain, AK & Jaiswal, AK (2009) Antioxidant-induced modification of INrf2 cysteine 151 and PKC-delta-mediated phosphorylation of Nrf2 serine 40 are both required for stabilization and nuclear translocation of Nrf2 and increased drug resistance. J Cell Sci 122, 44524464.
61. Nakajima, H, Nakajima-Takagi, Y, Tsujita, T, et al. (2011) Tissue-restricted expression of Nrf2 and its target genes in zebrafish with gene-specific variations in the induction profiles. PLoS ONE 6, e26884.
62. Boettler, U, Sommerfeld, K, Volz, N, et al. (2011) Coffee constituents as modulators of Nrf2 nuclear translocation and are (EpRE)-dependent gene expression. J Nutr Biochem 22, 426440.
63. Kang, M, Kobayashi, A, Wakabayashi, N, et al. (2004) Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc Natl Acad Sci USA 101, 20462051.
64. Blake, DJ, Singh, A, Kombairaju, P, et al. (2010) Deletion of Keap1 in the lung attenuates acute cigarette smoke–induced oxidative stress and inflammation. Am J Resp Cell Mol 42, 524536.
65. Lee, O, Jain, AK, Papusha, V, et al. (2007) An auto-regulatory loop between stress sensors INrf2 and Nrf2 controls their cellular abundance. J Biol Chem 282, 3641236420.
66. Martin-Liberal, J, Cameron, AJ, Claus, J, et al. (2014) Targeting protein kinase C in sarcoma. Biochim Biophys Acta 1846, 547559.
67. Gilio, K, Harper, MT, Cosemans, JM, et al. (2010) Functional divergence of platelet protein kinase C (PKC) isoforms in thrombus formation on collagen. J Biol Chem 285, 2341023419.
68. Bruewer, M, Luegering, A, Kucharzik, T, et al. (2003) Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 171, 61646172.
69. Umemura, A, Park, EJ, Taniguchi, K, et al. (2014) Liver damage, inflammation, and enhanced tumorigenesis after persistent mTORC1 inhibition. Cell Metab 20, 133144.
70. 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 Endocr 172, 494504.
71. 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, R727R739.
72. Krause, G, Winkler, L, Piehl, C, et al. (2009) Structure and function of extracellular claudin domains. Ann Ny Acad Sci 1165, 3443.
73. Krogdahl, Å, Bakke McKellep, AM & Baeverfjord, G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquacult Nutr 9, 361371.
74. Gao, D, Xu, ZE, Qiao, P, et al. (2013) Cadmium induces liver cell apoptosis through Caspase-3A activation in purse red common carp (Cyprinus carpio). PLOS ONE 8, e83423.
75. Sharifi, AM, Eslami, H, Larijani, B, et al. (2009) Involvement of caspase-8,-9, and-3 in high glucose-induced apoptosis in PC12 cells. Neurosci Lett 459, 4751.
76. Fast, MD, Johnson, SC & Jones, S (2007) Differential expression of the pro-inflammatory cytokines IL-1β-1, TNFα-1 and IL-8 in vaccinated pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon juveniles. Fish Shellfish Immun 22, 403407.
77. Tsukumo, Y, Laplante, M, Parsyan, A, et al. (2014) MTOR and regulation of translation. In Translation and Its Regulation in Cancer Biology and Medicine, pp. 307343 [A Parsyan, editor]. Dordrecht, The Netherlands: Springer.
78. Hu, K, Zhang, J, Feng, L, et al. (2015) Effect of dietary glutamine on growth performance, non-specific immunity, expression of cytokine genes, phosphorylation of target of rapamycin (TOR), and anti-oxidative system in spleen and head kidney of Jian carp (Cyprinus carpio var. Jian). Fish Physiol Biochem 41, 635649.
79. Tain, LS, Mortiboys, H, Tao, RN, et al. (2009) Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss. Nat Neurosci 12, 11291135.
80. Windmueller, HG (1982) Glutamine utilization by the small intestine. Adv Enzymol Relat Areas Mol Biol 53, 37.
81. Hu, K, Feng, L, Jiang, WD, et al. (2014) Oxidative damage repair by glutamine in fish enterocytes. Fish Physiol Biochem 40, 14371445.


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Soyabean glycinin depresses intestinal growth and function in juvenile Jian carp (Cyprinus carpio var Jian): protective effects of glutamine

  • Wei-Dan Jiang (a1) (a2) (a3), Kai Hu (a1) (a4), Jin-Xiu Zhang (a1), Yang Liu (a1) (a2) (a3), Jun Jiang (a1), Pei Wu (a1) (a2) (a3), Juan Zhao (a1), Sheng-Yao Kuang (a5), Ling Tang (a5), Wu-Neng Tang (a5), Yong-An Zhang (a6), Xiao-Qiu Zhou (a1) (a2) (a3) and Lin Feng (a1) (a2) (a3)...


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