Effect of OPG-supplemented diet on immune and stress responses and attenuation of LPS-induced damage in the liver of carp (Cyprinus carpio haematopterus)
DOI:
https://doi.org/10.20950/1678-2305/bip.2022.48.e734Resumo
Effects of oxidized peptidoglycan (OPG) on immune and stress responses and lipopolysaccharide (LPS)-induced damage in the liver of carp were investigated in this study. Four hundred carps (Cyprinus carpio haematopterus) were fed with five experimental diets supplemented with 0, 100, 200, 400, and 800 mg kg-1 OPG for 28 days. Each group had four replicates and 20 fish per replication. LPS challenge (injection of 40 mg kg-1 saline or LPS) occurred at day 29. The supplementation with OPG linearly increased (p<0.05) plasma total protein, immunoglobulin M (IgM), complement 4 (C4), cortisol, and lactate on day 14. Dietary supplementation with OPG linearly increased (p<0.05) plasma and complement 3 (C3); quadratically improved (p<0.05) alkaline phosphatase (ALP) and lysozyme (LYS) activities; linearly increased hepatic superoxide dismutase (SOD) and catalase (CAT) activities; increased malondialdehyde (MDA) contents; and improved (p<0.05) hepatic anti-superoxide anion (ASA) and anti-hydroxy radical (AHR) contents on days 14 and 28. Dietary OPG significantly prevented the increase of interleukin 1β (IL-1β), interleukin 6 (IL-6), and tumor necrosis factor α (TNF-α) by inhibiting the excessive activation of TLR2-Myd88 signaling pathway; downregulating TLR2, Myd88, and NF-κB p65; and upregulating nuclear factor erythroid-2-related factor 2 (Nrf2) and Keap1 mRNA expression (p<0.05). Therefore, this study indicated that dietary OPG improves the plasma immune response, regulates the hepatic antioxidant status, and attenuates LPS-induced negative effects in the carp at the optimal dose of 400 mg kg-1.
Referências
Angeles, D.M.; Liu, Y.; Hartman, A.M.; Borisova, M.; Borges, A.S.; Kok, N.D.; Beilharz, K.; Veening, J.W.; Mayer, C. 2017. Pentapeptide-rich peptidoglycan at the Bacillus subtilis cell-division site. Molecular Microbiology, 104(2): 319-333. https://doi.org/10.1111/mmi.13629
Armenteros, M.; Heinonen, M.; Ollilainen, V.; Toldrá, F.; Estévez, M. 2009. Analysis of protein carbonyls in meat products by using the DNPH-method, fluorescence spectroscopy and liquid chromatographye-electrospray ionisatione-mass spectrometry (LC-ESI-MS). Meat Science, 83(1): 104-112. https://doi.org/10.1016/j.meatsci.2009.04.007
Barka, T.; Anderson, P. 1962. Histochemical methods for acid phosphatase using hexazonium pararosanalin as coupler. Journal of Histochemistry & Cytochemistry, 10: 741-753.
Beeby, M.; Gumbart, J.C.; Roux, B.; Jensen, G.J. 2013. Architecture and assembly of the Gram-positive cell wall. Molecular Microbiology, 88(4): 664-672. https://doi.org/10.1111/mmi.12203
Beutler, E. 1975. Red cell metabolism: a manual of biochemical methods. New York: Grune Strottan.
Chen, X.M.; Wang, Q.J.; Guo, Z.X.; Zhao, Y.L.; Luo, S.; Yu, T.; Zhang, D.M.; Wang, G.Q. 2020. Identification of the Nrf2 in the fathead minnow muscle cell line: role for a regulation in response to H2O2 induced the oxidative stress in fish cell. Fish Physiology and Biochemistry, 46(5): 1699-1711. https://doi.org/10.1007/s10695-020-00822-8
China Society of Fisheries. 2020. China fisheries statistical yearbook. Beijing: China Agriculture Press.
Duan, X.D.; Feng, L.; Jiang, W.D.; Wu, P.; Liu, Y.; Kuang, S.Y.; Tang, L.; Tang, W.N.; Zhang, Y.A.; Zhou, X.Q. 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 signaling. Aquaculture Nutrition, 25(4): 770-782. https://doi.org/10.1111/anu.12895
Ellis, A. 1990. Techniques in fish immunology. Lysozyme Assays, 101-103.
Giri, S.S., Sen, S.S.; Chi, C.; Kim, H.J.; Yun, S.; Park, S.C. 2015a. Chlorophytum borivilianum polysaccharide fraction provokes the immune function and disease resistance of Labeo rohita against Aeromonas hydrophila. Journal of Immunology Research, 6;2015: 256510. https://doi.org/10.1155/2015/256510
Giri, S.S.; Sen, S.S.; Chi, C.; Kim, H.J.; Yun, S.; Park, S.C.; Sukumaran, V. 2015b. Effects of intracellular products of Bacillus subtilis VSG1 and Lactobacillus plantarum VSG3 on cytokine responses in the head kidney macrophages of Labeo rohita. Fish & Shellfish Immunology, 47(2): 954-961. https://doi.org/10.1016/j.fsi.2015.10.033
Hamann, L.; EL-Samalouti, V.; Ulmer, A.J.; Flad, H.D.; Rietschel, E.T. 1998. Components of gut bacteria as immunomodulators. International Journal of Food Microbiology, 41(2): 141-154. https://doi.org/10.1016/S0168-1605(98)00047-6
Hao, J.; Wu, F.; Tang, R.; Sun, Y.; Liu, D.; Zhang, Z. 2020. Preparation of 1,4-linked α-D-glucuronans from starch with 4-acetamide-TEMPO/NaClO2/NaClO system. International Journal of Biological Macromolecules, 151: 740-746. https://doi.org/10.1016/j.ijbiomac.2020.02.211
He, J.Y.; Wu, Z.; Pan, D.D.; Guo, Y.X.; Zen, X.Q. 2017. Effect of selenylation modification on antitumor activity of peptidoglycan from Lactobacillus acidophilus. Carbohydrate Polymers, 165: 344-350. https://doi.org/10.1016/j.carbpol.2017.02.031
Isogai, A.; Saito, T.; Fukuzumi, H. 2011. TEMPO-oxidized cellulose nanofibers. Nanoscale, 2011;3(1): 71-85. https://doi.org/10.1039/c0nr00583e
Jia, R.; Du, J.L.; Cao, L.P.; Li, Y.; Johnson, O.; Gu, Z.; Jeney, G.; Xu, P.; Yin, G. 2019. Antioxidative, inflammatory and immune responses in hydrogen peroxide-induced liver injury of tilapia (GIFT, Oreochromis niloticus). Fish & Shellfish Immunology, 84: 894-905. https://doi.org/10.1016/j.fsi.2018.10.084
Jiang, J.; Shi, D.; Zhou, X.Q.; Hu, Y.; Feng, L.; Liu, Y.; Jiang, W.D.; Zhao, Y. 2015. In vitro and in vivo protective effect of arginine against lipopolysaccharide induced inflammatory response in the intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Fish & Shellfish Immunology, 42(2): 457-464. https://doi.org/10.1016/j.fsi.2014.11.030
Lee, S.H.; Ingale, S.L.; Kim, J.S.; Kim, K.H.; Lokhande, A.; Kim, E.K.; Kwon, I.K.; Kim, Y.H.; Cha, B.J. 2014. Effects of dietary supplementation with Bacillus subtilis LS1–2 fermentation biomass on growth performance, nutrient digestibility, cecal microbiota and intestinal morphology of weanling pig. Animal Feed Science and Technology, 188: 102-110. https://doi.org/10.1016/j.anifeedsci.2013.12.001
Li, W.H.; Wang, L.; He, H.Y.; Chen, J.; Yu, Y.R. 2016. Expression of neutrophil gelatinase-associated lipocalin in low osmolar contrast-induced nephropathy in rats and the effect of Nacetylcysteine. Experimental and Therapeutic Medicine, 12(5): 3175-3180. https://doi.org/10.3892/etm.2016.3779
Liu, X.M.; Xu, Z.; Chang, X.Q.; Fang, J.K.H.; Song, J.; He, J.F.; Tai, Z.G.; Zhu, Q.G.; Hu, M.H. 2021. Enhanced immunity and hemocytes proliferation by three immunostimulants in tri-spine horseshoe crab Tachypleus tridentatus. Fish & Shellfish Immunology, 115: 112-123. https://doi.org/10.1016/j.fsi.2021.06.001
Livak, K.J.; Schmittgen, T.D. 2001. Analysis of relative gene expression data using realtime quantitative PCR and the 2∆∆CT method. Methods, 25(4): 402-408. https://doi.org/10.1006/meth.2001.1262
Manhar, A.K.; Bashir, Y.; Saikia, D.; Nath, D.; Gupta, K.; Konwar, B.K.; Kumar, N.; Namsa, N.D.; Mandal, M. 2017. Corrigendum to “Cellulolytic potential of probiotic Bacillus subtilis AMS6 isolated from traditional fermented soybean (Churpi): An in-vitro study with regards to application as an animal feed additive”. Microbiological Research, 198: 56-57. https://doi.org/10.1016/j.micres.2017.02.005
Matsumoto, S.; Hara, T.; Nagaoka, M.; Mike, A.; Mitsuyama, K.; Sako, T.; Yamamoto, M.; Kado, S.; Takada, T. 2009. A component of polysaccharide peptidoglycan complex on Lactobacillus induced an improvement of murine model of inflammatory bowel disease and colitis-associated cancer. Immunology, 128(1 Part 2): e170-e180. https://doi.org/10.1111/j.1365-2567.2008.02942.x
Ming, J.H.; Ye, J.Y.; Zhang, Y.X.; Xu, Q.Y.; Yang, X.; Shao, X.P.; Qiang, J.; Xu, P. 2020. Optimal dietary curcumin improved growth performance, and modulated innate immunity, antioxidant capacity and related genes expression of NF-κB and Nrf2 signaling pathways in grass carp (Ctenopharyngodon idella) after infection with Aeromonas hydrophila. Fish & Shellfish Immunology, 97: 540-553. https://doi.org/10.1016/j.fsi.2019.12.074
Pandeirada, C.O.; Merkx, D.W.H.; Janssen, H.G.; Westphal, Y.; Schols, H.A. 2021. TEMPO/NaClO2/NaOCl oxidation of arabinoxylans. Carbohydrate Polymers, 259: 117781. https://doi.org/10.1016/j.carbpol.2021.117781
Pionnier, N.; Falco, A.; Miest, J.; Frost, P.; Irnazarow, I.; Shrive, A. Hoole, D. 2013. Dietary β-glucan stimulate complement and C-reactive protein acute phase responses in common carp (Cyprinus carpio) during an Aeromonas salmonicida infection. Fish & Shellfish Immunology, 34(3): 819-831. https://doi.org/10.1016/j.fsi.2012.12.017
Reuter, G. 2001. The Lactobacillus and Bifidobacterium microflora of the human intestine: Composition and succession. Current Issues in Intestinal Microbiology, 2(2): 43-53. https://doi.org/10.1002/1097-0142(195701/02)10:13.0.CO;2-V
Sheng, Q. 2011. Extraction of Peptidoglycan from Bacillus subtilis and its effects on immune function of mice. Sichuan Agricultural University.
Shi, H.Y.; Guo, Y.M.; Liu, Y.; Shi, B.L.; Guo, X.Y.; Jin, L.; Yan, S.M. 2016. The in vitro effect of lipopolysaccharide on proliferation, inflammatory factors and antioxidant enzyme activity in bovine mammary epithelial cells. Animal Nutrition, 2(2): 99-104. https://doi.org/10.1016/j.aninu.2016.03.005
Silvestre, F. 2020. Signaling pathways of oxidative stress in aquatic organisms exposed to xenobiotics. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 333(6): 436-448. https://doi.org/10.1002/jez.2356
Takemura, A. 1993. Changes in an immunoglobulin M (IgM)-like protein during larval stages in tilapia, Oreochromis mossambicus. Aquaculture, 115(3-4): 233-241. https://doi.org/10.1016/0044-8486(93)90139-P
Tang, H.G.; Wu, T.X.; Zhao, Z.Y.; Pan, X.D. 2008. Effects of fish protein hydrolysate on growth performance and humoral immune response in large yellow croaker (Pseudosciaena crocea R.). Journal of Zhejiang University-Science B, 2008;9: 684-690. https://doi.org/10.1631/jzus.B0820088
Tiantian, Z.; Haicheng, Y.; Wei, H. 2019. Protective Effect of Bacillus subtilis Peptidoglycan (PG) on β-conglycinin-induced intestinal epithelial cells damage of juvenile carp (Cyprinus carpio). Animal Husbandry and Feed Science, 2019;11(2): 56-61. https://doi.org/10.19578/j.cnki.ahfs.2019.02.004
Wei, K.Q.; Yang, J.X.; Song, C.X. 2020. The responses of prophenoloxidase and MAPK/Nrf2 pathway to cadmium stress in red swamp crayfish Procambarus clarkii. Marine and Freshwater Behaviour and Physiology, 53(2): 59-72. https://doi.org/10.1080/10236244.2020.1764189
Wu, Z.; Pan, D.D.; Guo, Y.X.; Zeng, X.Q. 2013. Structure and anti-inflammatory capacity of peptidoglycan from Lactobacillus acidophilus in RAW-264.7 cells. Carbohydrate Polymers, 96(2): 466-473. https://doi.org/10.1016/j.carbpol.2013.04.028
Wu, Z.; Pan, D.D.; Zeng, X.Q.; Sun, Y.Y.; Cao, J.X. 2016. Phosphorylation of peptidoglycan from Lactobacillus acidophilus and its immunoregulatory function. International Journal of Food Science & Technology, 51(3): 664-671. https://doi.org/10.1111/ijfs.13028
Yu, Y.B.; Wang, C.H. Wang, A.M.; Yang, W.P.; Lv, F.; Liu, F.; Liu, B.; Sun, C.X. 2018. Effects of various feeding patterns of Bacillus coagulans on growth performance, antioxidant response and Nrf2-Keap1 signaling pathway in juvenile gibel carp (Carassius auratus gibelio). Fish & Shellfish Immunology, 73: 75-83. https://doi.org/10.1016/j.fsi.2017.11.050
Yu, Z.; Zheng, Y.G.; Du, H.L.; Li, H.J.; Wu, L.F. 2020. Bioflocs protects copper-induced inflammatory response and oxidative stress in Rhynchocypris lagowski Dybowski through inhibiting NF-κB and Nrf2 signaling pathways. Fish & Shellfish Immunology, 98: 466-476. https://doi.org/10.1016/j.fsi.2020.01.048
Zhang, X.D.; Zhu, Y.F.; Cai, L.S.; Wu, T.X. 2008. Effects of fasting on the meat quality and antioxidant defenses of market-size farmed large yellow croaker (Pseudosciaena crocea). Aquaculture, 280(1-4): 136-139. https://doi.org/10.1016/j.aquaculture.2008.05.010
Zhao, J.; Liu, Y.; Jiang, J.; Wu, P.; Jiang, W.D.; Li, S.H.; Tang, L.; Kuang, S.Y.; Feng, L.; Zhou, X.Q. 2013. Effects of dietary isoleucine on the immune response, antioxidant status and gene expression in the head kidney of juvenile Jian carp (Cyprinus carpio var. Jian). Fish & Shellfish Immunology, 35(2): 572-580. https://doi.org/10.1016/j.fsi.2013.05.027
Zhou, Z.X.; Lin, Z.J.; Pang, X.; Shan; P.P.; Wang, J.X. 2018. MicroRNA regulation of Toll-like receptor signaling pathways in teleost fish. Fish & Shellfish Immunology, 75: 32-40. https://doi.org/10.1016/j.fsi.2018.01.036
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