Abstract
The study investigated the effects of dietary isoleucine (Ile) on skin mucus barrier and epithelial physical barrier functions of hybrid bagrid catfish Pelteobagrus vachelli × Leiocassis longirostris. A total of 630 fish (33.11 ± 0.09 g) were fed semi-purified isonitrogenous diets containing 5.0 (control), 7.5, 10.0, 12.5, 15.0, 17.5, and 20.0 g Ile kg −1 diet for 8 weeks. The results indicated that dietary Ile increased (P < 0.05) in skin (1) mucus protein content and antimicrobial activity against three gram-negative bacteria (Aeromonas hydrophila, Escherichia coli, and Yersinia ruckeri) and two gram-positive bacteria (Streptococcus agalactiae and Staphylococcus aureus), (2) mucus lysofew information is available about the influencezyme (LZM), acid phosphatase (ACP), and alkaline phosphatase (AKP) activities, and complement 3 and 4 (C3 and C4) and immunoglobulin M (IgM) contents, (3) intelectin 1 (intl1), intelectin 2 (intl2), c-type-lysozyme (c-LZM), g-type-lysozyme (g-LZM), and β-defensin mRNA levels. Dietary Ile decreased (P < 0.05) reactive oxygen species (ROS), malondialdehyde (MDA), and protein carbonyl (PC) contents, and up-regulated (P < 0.05) CuZnSOD, GST, GPX1a, muc5ac, muc5b, zonula occludens-1 (ZO-1), zonula occludens-2 (ZO-2), occludin, and claudin 3 mRNA levels in skin. These results indicated that Ile improved skin mucus barrier function via increasing mucus protein, C3 and C4, and IgM contents and antibacterial factors activities, and promoted epithelial physical barrier function via decreasing skin antioxidant damage and improving tight junction structure in hybrid bagrid catfish.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A Mol Integr Physiol 138(4):405–415. https://doi.org/10.1016/j.cbpb.2004.05.013
Adamek M, Syakuri H, Harris S, Rakus KA, Brogden G, Matras M, Irnazarow I, Steinhagen D (2013) Cyprinid herpesvirus 3 infection disrupts the skin barrier of common carp (Cyprinus carpio L.). Vet Microbiol 162(2):456–470. https://doi.org/10.1016/j.vetmic.2012.10.033
Adel M, Amiri AA, Zorriehzahra J, Nematolahi A, Esteban MÁ (2015) Effects of dietary peppermint (Mentha piperita) on growth performance, chemical body composition and hematological and immune parameters of fry Caspian white fish (Rutilus frisii kutum). Fish Shellfish Immun 45(2):841–847. https://doi.org/10.1016/j.fsi.2015.06.010
Amasheh S, Meiri N, Gitter AH, Schöneberg T, Mankertz J, Schulzke JD, Fromm M (2002) Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 115(24):4969–4976. https://doi.org/10.1242/jcs.00165
Azzam MMM, Zou XT, Dong XY, Xie P (2011) Effect of supplemental L-threonine on mucin 2 gene expression and intestine mucosal immune and digestive enzymes activities of laying hens in environments with high temperature and humidity. Poultry Sci 90(10):2251–2256. https://doi.org/10.3382/ps.2011-01574
Bansil R, Turner BS (2018) The biology of mucus: composition, synthesis and organization. Adv Drug Deliver Rev 124:3–15. https://doi.org/10.1016/j.addr.2017.09.023
Benhamed S, Guardiola FA, Mars M, Esteban MÁ (2014) Pathogen bacteria adhesion to skin mucus of fishes. Vet Microbiol 171(1):1–12. https://doi.org/10.1016/j.vetmic.2014.03.008
Berdikova Bohne VJ, 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(5):733–746. https://doi.org/10.1016/j.fct.2006.10.020
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(1):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brinchmann MF (2016) Immune relevant molecules identified in the skin mucus of fish using -omics technologies. Mol BioSyst 12(7):2056–2063
Chang MX, Nie P (2007) Intelectin gene from the grass carp Ctenopharyngodon idella: cDNA cloning, tissue expression, and immunohistochemical localization. Fish Shellfish Immun 23(1):128–140. https://doi.org/10.1016/j.fsi.2006.09.012
Chen K, Jiang W, Wu P, Liu Y, Kuang S, Tang L, Tang W, Zhang Y, Zhou X, Feng L (2017) Effect of dietary phosphorus deficiency on the growth, immune function and structural integrity of head kidney, spleen and skin in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immun 63:103–126. https://doi.org/10.1016/j.fsi.2017.02.007
Chu HW, Balzar S, Seedorf GJ, Westcott JY, Trudeau JB, Silkoff P, Wenzel SE (2004) Transforming growth factor-β2 induces bronchial epithelial mucin expression in asthma. Am J Pathol 165(4):1097–1106. https://doi.org/10.1016/S0002-9440(10)63371-8
Dong XY, Azzam MMM, Zou XT (2016) Effects of dietary L-isoleucine on laying performance and immunomodulation of laying hens. Poultry Sci 95(10):2297–2305. https://doi.org/10.3382/ps/pew163
Esteban M (2012) An overview of the immunological defenses in fish skin. ISRN Immunol 201:21–29. https://doi.org/10.5402/2012/853470
Feng L, Gan L, Jiang W, Wu P, Liu Y, Jiang J, Tang L, Kuang S, Tang W, Zhang Y, Zhou X (2017) Gill structural integrity changes in fish deficient or excessive in dietary isoleucine: towards the modulation of tight junction protein, inflammation, apoptosis and antioxidant defense via NF-κB, TOR and Nrf2 signaling pathways. Fish Shellfish Immun 63:127–138. https://doi.org/10.1016/j.fsi.2017.02.010
Guardiola FA, Cuesta A, Abellán E, Meseguer J, Esteban MA (2014) Comparative analysis of the humoral immunity of skin mucus from several marine teleost fish. Fish Shellfish Immun 40(1):24–31. https://doi.org/10.1016/j.fsi.2014.06.018
He P, Jiang WD, Liu XA, Feng L, Wu P, Liu Y, Jiang J, Tan BP, Yang QH, Kuang SY, Tang L, Zhou XQ (2020) Dietary biotin deficiency decreased growth performance and impaired the immune function of the head kidney, spleen and skin in on-growing grass carp (Ctenopharyngodon idella). Fish Shellfish Immun 97:216–234. https://doi.org/10.1016/j.fsi.2019.12.033
Hoseinifar SH, Sharifian M, Vesaghi MJ, Khalili M, Esteban MÁ (2014) The effects of dietary xylooligosaccharide on mucosal parameters, intestinal microbiota and morphology and growth performance of Caspian white fish (Rutilus frisii kutum) fry. Fish Shellfish Immun 39(2):231–236. https://doi.org/10.1016/j.fsi.2014.05.009
Jiang J, Shi D, Zhou X, Yin L, Feng L, Liu Y, Jiang W, Zhao Y (2015) Effects of glutamate on growth, antioxidant capacity, and antioxidant-related signaling molecule expression in primary cultures of fish enterocytes. Fish Physiol Biochem 41(5):1143–1153. https://doi.org/10.1007/s10695-015-0076-3
Jiang WD, Xu J, Zhou XQ, Wu P, Liu Y, Jiang J, Kuang SY, Tang L, Tang WN, Zhang YA, Feng L (2017a) Dietary protein levels regulated antibacterial activity, inflammatory response and structural integrity in the head kidney, spleen and skin of grass carp (Ctenopharyngodon idella) after challenged with Aeromonas hydrophila. Fish Shellfish Immun 68:154–172. https://doi.org/10.1016/j.fsi.2017.07.019
Jiang J, Yin L, Li J, Li Q, Shi D, Feng L, Liu Y, Jiang W, Wu P, Zhao Y, Zhou X (2017b) Glutamate attenuates lipopolysaccharide-induced oxidative damage and mRNA expression changes of tight junction and defensin proteins, inflammatory and apoptosis response signaling molecules in the intestine of fish. Fish Shellfish Immun 70:473–484. https://doi.org/10.1016/j.fsi.2017.09.035
Jin Y, Zheng S, Pu Y, Shu L, Sun L, Liu W, Fu Z (2011) Cypermethrin has the potential to induce hepatic oxidative stress, DNA damage and apoptosis in adult zebrafish (Danio rerio). Chemosphere 82(3):398–404. https://doi.org/10.1016/j.chemosphere.2010.09.072
Jobling M (2011) National Research Council (NRC): nutrient requirements of fish and shrimp. Aquac Int 20(3):601–602. https://doi.org/10.1007/s10499-011-9480-6
Kania PW, Sorensen RR, Koch C, Brandt J, Kliem A, Vitved L, Hansen S, Skjodt K (2010) Evolutionary conservation of mannan-binding lectin (MBL) in bony fish: identification, characterization and expression analysis of three bona fide collectin homologues of MBL in the rainbow trout (Onchorhynchus mykiss). Fish Shellfish Immun 29(6):910–920. https://doi.org/10.1016/j.fsi.2010.07.020
Ke F, Wang Y, Cao X, Pan G, Geng R (2016) Cloning and expression analysis of c-type and g-type lysozymes in yellow catfish (Pelteobagrus fulvidraco). Genes Genom 38(8):707–716. https://doi.org/10.1007/s13258-016-0414-6
Kirschner N, Brandner JM (2012) Barriers and more: functions of tight junction proteins in the skin. Ann N Y Acad Sci 1257(1):158–166. https://doi.org/10.1111/j.1749-6632.2012.06554.x
Ko JY, Kim EA, Lee JH, Kang MC, Lee JS, Kim JS, Jung WK, Jeon YJ (2014) Protective effect of aquacultured flounder fish-derived peptide against oxidative stress in zebrafish. Fish Shellfish Immun 36(1):320–323. https://doi.org/10.1016/j.fsi.2013.11.018
Krishnaswamy K, Gopalan C (1971) Effect of isoleucine on skin and electroencephalogram in pellagra. Lancet 298(7735):1167–1169. https://doi.org/10.1016/S0140-6736(71)90486-7
Li J, Liang X, Tan Q, Yuan X, Liu L, Zhou Y, Li B (2014) Effects of vitamin E on growth performance and antioxidant status in juvenile grass carp Ctenopharyngodon idellus. Aquaculture 430:21–27. https://doi.org/10.1016/j.aquaculture.2014.03.019
Mansouri Taee H, Hajimoradloo A, Hoseinifar SH, Ahmadvand H (2017) Dietary Myrtle (Myrtus communis L.) improved non-specific immune parameters and bactericidal activity of skin mucus in rainbow trout (Oncorhynchus mykiss) fingerlings. Fish Shellfish Immun 64:320–324. https://doi.org/10.1016/j.fsi.2017.03.034
Marseglia A, Licari A, Agostinis F, Barcella A, Bonamonte D, Puviani M, Milani M, Marseglia G (2014) Efficacy of a rhamnosoft, ceramides, and L-isoleucine cream in atopic eczema of the face: a randomized controlled trial. Pediatr Allergy Immunol 25:271–275. https://doi.org/10.1111/pai.12185
Mckenzie JD, Grigolava IV (1996) The echinoderm surface and its role in preventing microfouling. Biofouling 10(1–3):261–272. https://doi.org/10.1080/08927019609386285
Micallef G, Bickerdike R, Meharg C, Fernandes J, Bowman A, Martin S (2012) Exploring the transcriptome of Atlantic salmon (Salmo salar) skin, a major defense organ. Mar Biotechnol 14(5):559–569. https://doi.org/10.1007/s10126-012-9447-2
Palaksha KJ, Shin G, Kim Y, Jung T (2008) Evaluation of non-specific immune components from the skin mucus of olive flounder (Paralichthys olivaceus). Fish Shellfish Immun 24(4):479–488. https://doi.org/10.1016/j.fsi.2008.01.005
Patel RM, Myers LS, Kurundkar AR, Maheshwari A, Nusrat A, Lin PW (2012) Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am J Pathol 180(2):626–635. https://doi.org/10.1016/j.ajpath.2011.10.025
Petro TM, Bhattacharjee JK (1980) Effect of dietary essential amino acid limitations upon native levels of murine serum immunoglobulins, transferrin, and complement. Infect Immun 27(2):513–518
Rahimnejad S, Lee K (2014) Dietary isoleucine influences non-specific immune response in juvenile olive flounder (Paralichthys olivaceus). Turk J Fish Aquat Sci 14:853–862. https://doi.org/10.4194/1303-2712-v14_4_02
Raj VS, Fournier G, Rakus K, Ronsmans M, Ouyang P, Michel B, Delforges C, Costes B, Farnir F, Leroy B, Wattiez R, Melard C, Mast J, Lieffrig F, Vanderplasschen A (2011) Skin mucus of Cyprinus carpio inhibits cyprinid herpesvirus 3 binding to epidermal cells. Vet Res 42(1):92. https://doi.org/10.1186/1297-9716-42-92
Ren M, Zhang S, Liu X, Li S, Mao X, Zeng X, Qiao S (2016) Different lipopolysaccharide branched-chain amino acids modulate porcine intestinal endogenous β-defensin expression through the Sirt1/ERK/90RSK pathway. J Agr Food Chem 64(17):3371–3379. https://doi.org/10.1021/acs.jafc.6b00968
Rhee J, Yu IT, Kim B, Jeong C, Lee K, Kim M, Lee S, Park GS, Lee J (2013) Copper induces apoptotic cell death through reactive oxygen species-triggered oxidative stress in the intertidal copepod Tigriopus japonicus. Aquat Toxicol 132-133:182–189. https://doi.org/10.1016/j.aquatox.2013.02.013
Roosta Z, Hajimoradloo A, Ghorbani R, Hoseinifar SH (2014) The effects of dietary vitamin C on mucosal immune responses and growth performance in Caspian roach (Rutilus rutilus caspicus) fry. Fish Physiol Biochem 40(5):1601–1607. https://doi.org/10.1007/s10695-014-9951-6
Safari R, Hoseinifar SH, Van Doan H, Dadar M (2017) The effects of dietary Myrtle (Myrtus communis) on skin mucus immune parameters and mRNA levels of growth, antioxidant and immune related genes in zebrafish (Danio rerio). Fish Shellfish Immun 66:264–269. https://doi.org/10.1016/j.fsi.2017.05.007
Sanahuja I, Fernández-Alacid L, Ordóñez-Grande B, Sánchez-Nuño S, Ramos A, Araujo RM, Ibarz A (2019) Comparison of several non-specific skin mucus immune defences in three piscine species of aquaculture interest. Fish Shellfish Immun 89:428–436. https://doi.org/10.1016/j.fsi.2019.04.008
Sun YZ, Yang HL, Ma RL, Lin WY (2010) Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish Shellfish Immun 29(5):803–809. https://doi.org/10.1016/j.fsi.2010.07.018
Takano T, Sha Z, Peatman E, Terhune J, Liu H, Kucuktas H, Li P, Edholm E, Wilson M, Liu Z (2008) The two channel catfish intelectin genes exhibit highly differential patterns of tissue expression and regulation after infection with Edwardsiella ictaluri. Dev Comp Immunol 32(6):693–705. https://doi.org/10.1016/j.dci.2007.10.008
Thomas LA, Hermans CO (1985) Adhesive interactions between the tube feet of a starfish, Leptasterias Hexactis and substrata. Biol Bull 169(3):675–688. https://doi.org/10.2307/1541309
Van der Marel M, Adamek M, Gonzalez SF, Frost P, Rombout JHWM, Wiegertjes GF, Savelkoul HFJ, Steinhagen D (2012) Molecular cloning and expression of two β-defensin and two mucin genes in common carp (Cyprinus carpio L.) and their up-regulation after β-glucan feeding. Fish Shellfish Immun 32(3):494–501. https://doi.org/10.1016/j.fsi.2011.12.008
Vennila R, Kumar KR, Kanchana S, Arumugam M, Vijayalakshmi S, Balasubramaniam T (2011) Preliminary investigation on antimicrobial and proteolytic property of the epidermal mucus secretion of marine stingrays. Asian Pacif J Tropic Biomed 1(2, supplement):S239–S243. https://doi.org/10.1016/S2221-1691(11)60162-7
Wang G, Xu Q, Jin X, Hang F, Liu Z, Zhao J, Zhang H, Chen W (2018) Effects of lactobacilli with different regulatory behaviours on tight junctions in mice with dextran sodium sulphate-induced colitis. J Funct Foods 47:107–115. https://doi.org/10.1016/j.jff.2018.05.044
Xiong Y, Dan C, Ren F, Su ZH, Zhang YB, Mei J (2020) Proteomic profiling of yellow catfish (Pelteobagrus fulvidraco) skin mucus identifies differentially-expressed proteins in response to Edwardsiella ictaluri infection. 100:98-108. https://doi.org/10.1016/j.fsi.2020.02.059
Xu J, Wu P, Jiang W, Liu Y, Jiang J, Kuang S, Tang L, Tang W, Zhang Y, Zhou X, Feng L (2016) Optimal dietary protein level improved growth, disease resistance, intestinal immune and physical barrier function of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immun 55:64–87. https://doi.org/10.1016/j.fsi.2016.05.021
Ye X, Zhang L, Tian Y, Tan A, Bai J, Li S (2010) Identification and expression analysis of the g-type and c-type lysozymes in grass carp Ctenopharyngodon idellus. Dev Comp Immunol 34(5):501–509. https://doi.org/10.1016/j.dci.2009.12.009
Zhao J, Liu Y, Jiang J, Wu P, Jiang W, Li S, Tang L, Kuang S, Feng L, Zhou X (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 Immun 35(2):572–580. https://doi.org/10.1016/j.fsi.2013.05.027
Zhao J, Feng L, Liu Y, Jiang W, Wu P, Jiang J, Zhang Y, Zhou X (2014) Effect of dietary isoleucine on the immunity, antioxidant status, tight junctions and microflora in the intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immun 41(2):663–673. https://doi.org/10.1016/j.fsi.2014.10.002
Zhao Y, Li J, Yin L, Feng L, Liu Y, Jiang W, Wu P, Zhao J, Chen D, Zhou X, Jiang J (2019) Effects of dietary glutamate supplementation on flesh quality, antioxidant defense and gene expression related to lipid metabolism and myogenic regulation in Jian carp (Cyprinus carpio var. Jian). Aquaculture 502:212–222. https://doi.org/10.1016/j.aquaculture.2018.12.050
Zhao Y, Li J, Jiang Q, Zhou X, Feng L, Liu Y, Jiang W, Wu P, Zhou J, Zhao J, Jiang J (2020) Leucine improved growth performance, muscle growth, and muscle protein deposition through AKT/TOR and AKT/FOXO3a signaling pathways in hybrid catfish Pelteobagrus vachelli × Leiocassis longirostris. Cells 9:327. https://doi.org/10.3390/cells9020327
Zhenyukh O, Civantos E, Ruiz-Ortega M, Sánchez MS, Vázquez C, Peiró C, Egido J, Mas S (2017) High concentration of branched-chain amino acids promotes oxidative stress, inflammation and migration of human peripheral blood mononuclear cells via mTORC1 activation. Free Radical Bio Med 104:104165–104177. https://doi.org/10.1016/j.freeradbiomed.2017.01.009
Zhong JR, Feng L, Jiang WD, Wu P, Liu Y, Jiang J, Kuang SY, Tang L, Zhou XQ (2019) Phytic acid disrupted intestinal immune status and suppressed growth performance in on-growing grass carp (Ctenopharyngodon idella). Fish Shellfish Immun 92:536–551. https://doi.org/10.1016/j.fsi.2019.06.045
Zhou T, Wang T, Garcia JGN (2014) Genes influenced by the non-muscle isoform of myosin light chain kinase impact human cancer prognosis. PLoS One 9(4):e94325. https://doi.org/10.1371/journal.pone.0094325
Zhou T, Liu S, Geng X, Jin Y, Jiang C, Bao L, Yao J, Zhang Y, Zhang J, Sun L, Wang X, Li N, Tan S, Liu Z (2017) GWAS analysis of QTL for enteric septicemia of catfish and their involved genes suggest evolutionary conservation of a molecular mechanism of disease resistance. Mol Gen Genomics 292(1):231–242. https://doi.org/10.1007/s00438-016-1269-x
Acknowledgements
This study was financially supported by National Natural Science Foundation of China (31702362) and National Key R&D Program of China (2018YFD0900400).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yin, L., Zhao, Y., Zhou, XQ. et al. Effect of dietary isoleucine on skin mucus barrier and epithelial physical barrier functions of hybrid bagrid catfish Pelteobagrus vachelli × Leiocassis longirostris. Fish Physiol Biochem 46, 1759–1774 (2020). https://doi.org/10.1007/s10695-020-00826-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-020-00826-4