Abstract
The heavy metal lead (Pb) is a contaminant widely distributed in the food chain. In this study, eight weeks of feeding containing Garlic (Allium sativum) or Fu-ling (Poria cocos) or both, markedly increased the growth index, enzyme activity, and serum index and significantly decreased muscle Pb level in grass carp (Ctenopharyngodon idella). Upon Pb exposure, the feeding Garlic or Fu-ling or both possessed the similar effects on improving the function of the antioxidant system and chelating ability. Further, the gene expressions of metal binding proteins (TF and MT-2) in the liver of the three experimental groups were significantly higher than those of the control group, which were all highly up-regulated after Pb exposure. At the same time, the activities of antioxidant enzymes (SOD and CAT) and the content of non-enzymatic substance (GSH) in the liver of the Garlic group, Fu-ling group and mixed group were stable compared to the control group after Pb exposure. Moreover, the reduction of Pb toxicity was manifested by the decrease of Pb content in the muscle, and the stable expression of heat stress proteins (HSP30 and HSP60) and immune-related genes (TNF-α and IL-1β). Taken together, the study preliminarily shows that the Garlic and Fu-ling play a role in mitigating the toxicity of Pb in grass carp.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Data and materials are available upon request.
References
Abd El-Hack ME, Abdelnour SA, Abd El-Moneim AEE, Arif M, Khafaga A, Shaheen H, Samak D, Swelum AA (2019) Putative impacts of phytogenic additives to ameliorate lead toxicity in animal feed. Environ Sci Pollut R 26:23209–23218. https://doi.org/10.1007/s11356-019-05805-8
Al osman M, Yang F, Massey IY (2019) Exposure routes and health effects of heavy metals on children. Biometals 32:563–573. https://doi.org/10.1007/s10534-019-00193-5
Alves LC, Glover CN, Wood CM (2006) Dietary Pb accumulation in juvenile freshwater rainbow trout (Oncorhynchus mykiss). Arch Environ Con Tox 51:615–625. https://doi.org/10.1007/s00244-005-0212-7
Amirkolaie AK, Karimzadeh J, Kenari AA (2014) The effects of organic selenium on performance and oxidative level in rainbow trout (Oncorhynchus mykiss, Walbaum, 1792) fed a high-fat diet. J Anim Feed Sci 23:90–96. https://doi.org/10.22358/jafs/65721/2014
Angles-Cano E (1997) Structural basis for the pathophysiology of lipoprotein(a) in the athero-thrombotic process. Braz J Med Biol Res 30:1271–1280. https://doi.org/10.1590/s0100-879x1997001100002
Anjiki N, Hoshino R, Ohnishi Y, Hioki K, Irie Y, Ishige A, Watanabe K (2005) A Kampo formula Juzen-taiho-to induces expression of metallothioneins in mice. Phytother Res 19:10. https://doi.org/10.1002/ptr.1747
Ates B, Orun I, Talas ZS, Durmaz G, Yilmaz I (2008) Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb2+ and Cu2+. Fish Physiol Biochem 34:53–59. https://doi.org/10.1007/s10695-007-9146-5
Awad E, Awaad A (2017) Role of medicinal plants on growth performance and immune status in fish. Fish shellfish immunol 67:40–54. https://doi.org/10.1016/j.fsi.2017.05.034
Berbert DM, Queiroz, EC, Melo EC (2005) Official methods of analysis of AOAC international, eighteenth ed., (2005) USA. https://doi.org/10.1016/0924-2244(95)90022-5
Boshuizen M, Van DPK, Von BL, Biemond BJ, Zeerleder SS, Bruggen VR, Juffermans NP (2017) Therapeutic use of transferrin to modulate anemia and conditions of iron toxicity. Blood Rev 31:400–405. https://doi.org/10.1016/j.blre.2017.07.005
Cai CY, Chen YC, Zhong SP, Zhang YM, Jiang JY, Xu H, Shi GG (2016) Synergistic effect of compounds from a Chinese herb: compatibility and dose optimization of compounds from N-butanol extract of Ipomoea stolonifera. Sci Rep-Uk 6. https://doi.org/10.1038/Srep27014
Cai Y, Yin Y, Wang L, Leng D, Ge C, Abdallah A, Li Y (2019) Effect on serum parameters and immune responses of Carassius auratus gibelio exposed to dietary lead and Bacillus subtilis. Biol Trace Elem Res 190. https://doi.org/10.1007/s12011-018-1544-2
Chen L, Feng L, Jiang WD, Jiang J, Wu P, Zhao J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Liu Y (2015) Dietary riboflavin deficiency decreases immunity and antioxidant capacity, and changes tight junction proteins and related signaling molecules mRNA expression in the gills of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 45:307–320. https://doi.org/10.1016/j.fsi.2015.04.004
Chen YY, Chang HM (2004) Antiproliferative and differentiating effects of polysaccharide fraction from fu-ling (Poria cocos) on human leukemic U937 and HL-60 cells. Food Chem Toxicol 42:759–769. https://doi.org/10.1016/j.fct.2004.01.018
Cheung APL, Lam THJ, Chan KM (2004) Regulation of Tilapia metallothionein gene expression by heavy metal ions. Mar Environ Res 58:389–394. https://doi.org/10.1016/j.marenvres.2004.03.084
Chung LY (2006) The antioxidant properties of garlic compounds: Allyl cysteine, alliin, allicin, and allyl disulfide. J Med Food 9:205–213. https://doi.org/10.1089/jmf.2006.9.205
Clausen CA, Iii FG, Woodward BM, Evans JW, DeGroot RC (2000) Correlation between oxalic acid production and copper tolerance in Wolfiporia cocos. Int Biodeter Biodegr 46:69–76. https://doi.org/10.1016/S0964-8305(00)00044-5
Connor T, Brewer C, Kelly J, Harkin A (2005) Acute stress suppresses pro-inflammatory cytokines TNF-α and IL-1β independent of a catecholamine-driven increase in IL-10 production. J Neuroimmunol 159:119–128. https://doi.org/10.1016/j.jneuroim.2004.10.016
Dai J, Zhang LB, Du XY, Zhang PJ, Li W, Guo XY, Li YH (2018) Effect of Lead on antioxidant ability and immune responses of crucian carp. Biol Trace Elem Res 186:546–553. https://doi.org/10.1007/s12011-018-1316-z
Dai W, Du HH, Fu LL, Jin CG, Xu ZR, Liu HT (2009) Effects of dietary Pb on accumulation, histopathology, and digestive enzyme activities in the digestive system of tilapia (Oreochromis niloticus). Biol Trace Elem Res 127:124–131. https://doi.org/10.1007/s12011-008-8227-3
De VG, Guida V, Carella F (2018) Urtica dioica (Stinging Nettle): a neglected plant with emerging growth promoter/immunostimulant properties for farmed Fish Front Physiol 9. https://doi.org/10.3389/Fphys.2018.00285
Dziegielewska K, Møller JE, Potter AM, Ek C, Lane M, Saunders N (2000) Acute-phase cytokines IL-1β and TNF-α in brain development. Cell Tissue Res 299:335–345. https://doi.org/10.1007/s004419900157
Ebokaiwe AP, Omaka ON, Okorie U, Oje O, Egedeigwe C, Ekwe A, Nnaji NJ (2018) Assessment of heavy metals around Abakaliki metropolis and potential bioaccumulation and biochemical effects on the liver, kidney, and erythrocyte of rats. Hum Ecol Risk Assess 24:1233–1255. https://doi.org/10.1080/10807039.2017.1410695
Farombi O, Adelowo OA, Ajimoko YR (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. Int J Environ Res Public Health 4:158–165. https://doi.org/10.3390/ijerph2007040011
Fu SL, Ding MM, Liang QJ, Yang YJ, Chen M, Wei XF, Wang AL, Liao SA, Ye JM (2019) The key differentially expressed genes and proteins related to immune response in the spleen of pufferfish (Takifugu obscurus) infected by Aeromonas hydrophila. Fish Shellfish Immunol 91:1–11. https://doi.org/10.1016/j.fsi.2019.05.016
Fu SL, Ding MM, Yang YJ, Kong JR, Li Y, Guo Z, Wang AL, Ye JM (2018) Molecular cloning, characterization and expression analysis of caspase-6 in puffer fish (Takifugu obscurus). Aquaculture 490:311–320. https://doi.org/10.1016/j.aquaculture.2018.03.008
Hahn SH, Yoo OJ, Gahl WA (2001) Effect of metal ions on the stability of metallothionein in the degradation by cellular fractions in vitro. Exp Mol Med 33:32–36. https://doi.org/10.1038/Emm.2001.7
Hossain M, Furuichi M (1999) Necessity of dietary calcium supplement in black sea bream. Fisheries Sci 65:893–897. https://doi.org/10.2331/fishsci.65.893
Hu T, Song JJ, Zeng WY, Li J, Wang HW, Zhang Y, Suo HY (2020) Lactobacillus plantarum LP33 attenuates Pb-induced hepatic injury in rats by reducing oxidative stress and inflammation and promoting Pb excretion. Food Chem Toxicol 143. https://doi.org/10.1016/J.Fct.2020.111533
Hwang IK, Kim KW, Kim JH, Kang JC (2016) Toxic effects and depuration after the dietary lead (II) exposure on the bioaccumulation and hematological parameters in starry flounder (Platichthys stellatus). Environ Toxicol Phar 45:328–333. https://doi.org/10.1016/j.etap.2016.06.017
İlyas T, Hanefi Ö, Cevat T, İsmail U (2003) The serum levels of IL-1β, IL-6, IL-8 and TNF-α in nonalcoholic fatty liver. Turk J Med Sci 381-386. https://journals.tubitak.gov.tr/medical/issues/sag-03-33-6/sag-33-6-7-0302-3.pdf
Iwama GK, Thomas PT, Forsyth RB, Vijayan MM (1998) Heat shock protein expression in fish. Rev Fish Bio Fisher 8:35–56. https://doi.org/10.1023/A:1008812500650
Jaiswal A, Verma A, Jaiswal P (2018) Detrimental effects of heavy metals in soil, plants, and aquatic ecosystems and in humans. J Environ Pathol Tox 37:183–197
Jing H, Zhang Q, Li S, Gao XJ (2020) Pb exposure triggers MAPK-dependent inflammation by activating oxidative stress and miRNA-155 expression in carp head kidney. Fish Shellfish Immunol 106:219–227. https://doi.org/10.1016/j.fsi.2020.08.015
Johansson MEV, Hansson GC (2014) Is the intestinal goblet cell a major immune cell. Cell Host Microbe 15:251–252. https://doi.org/10.1016/j.chom.2014.02.014
John WG, Wensheng S, Jennifer J, Ashley B, David C, Salim V, Eric B, Christie MB, Ron CH (2012) Abstract 166: small dense LDL cholesterol is associated with risk for coronary heart disease: The atherosclerosis risk in communities (ARIC) study. Arterioscler Thromb Vasc Biol 166
Kahlon SK, Sharma G, Julka JM, Kumar A, Sharma S, Stadler FJ (2018) Impact of heavy metals and nanoparticles on aquatic biota. Environ. Chem. Lett. 16:919–946. https://doi.org/10.1007/s10311-018-0737-4
Khan I, Huang G, Li X, Leong W, Xia W, Hsiao WLW (2018) Mushroom polysaccharides from Ganoderma lucidum and Poria cocos reveal prebiotic functions. J Funct Foods 41:191–201. https://doi.org/10.1016/j.jff.2017.12.046
Khan M, Samrana S, Zhang Y, Malik Z, Khan MD, Zhu SJ (2020) Reduced glutathione protects subcellular compartments from Pb-induced ROS injury in leaves and roots of upland cotton (Gossypium hirsutum L.). Front Plant Sci 11. https://doi.org/10.3389/Fpls.2020.00412
Kielian T, Bearden ED, Baldwin AC, Esen N (2004) IL-1 and TNF-alpha play a pivotal role in the host immune response in a mouse model of Staphylococcus aureus-induced experimental brain abscess. J Neuropath Exp Neur 63:381–396. https://doi.org/10.1093/jnen/63.4.381
Kim HJ, Mahboob S, Viayaraghavan P, Al-Ghanim KA, Al-Misned F, Kim YO, Ahmed Z (2020) Determination of toxic effects of lead acetate on different sizes of zebra fish (Danio rerio) in soft and hard water. J King Saud Univ Sci 32:1390–1394. https://doi.org/10.1016/j.jksus.2019.11.032
Kim JH, Kang JC (2015) The lead accumulation and hematological findings in juvenile rock fish Sebastes schlegelii exposed to the dietary lead (II) concentrations. Ecotox Environ Safe 115:33–39. https://doi.org/10.1016/j.ecoenv.2015.02.009
Kim JH, Park HJ, Kim KW, Hwang IK, Kim DH, Oh CW, Lee JS, Kang JC (2017) Growth performance, oxidative stress, and non-specific immune responses in juvenile sablefish, Anoplopoma fimbria, by changes of water temperature and salinity. Fish Physiol Biochem 43:1421–1431. https://doi.org/10.1007/s10695-017-0382-z
Kim MA, Williams KA (2017) Lead levels in landfill areas and childhood exposure: an integrative review. Public Health Nurs 34:87–97. https://doi.org/10.1111/phn.12249
Kumar VM, Henley AK, Nelson CJ, Indumati O, Rao YP, Rajanna S, Rajanna B (2017) Protective effect of Allium sativum (garlic) aqueous extract against lead-induced oxidative stress in the rat brain, liver, and kidney. Environ Sci Pollut R 24:1544–1552. https://doi.org/10.1007/s11356-016-7923-3
Lawal AO, Ellis EM (2011) The chemopreventive effects of aged garlic extract against cadmium-induced toxicity. Environ Toxicol Phar 32:266–274. https://doi.org/10.1016/j.etap.2011.05.012
Leblanc S, Hoglund E, Gilmour KM, Currie S (2012) Hormonal modulation of the heat shock response: insights from fish with divergent cortisol stress responses. Am J Physiol-Reg I 302:184–192. https://doi.org/10.1152/ajpregu.00196.2011
Lee JW, Choi H, Hwang UK, Kang JC, Kang YJ, Kim KI, Kim JH (2019) Toxic effects of lead exposure on bioaccumulation, oxidative stress, neurotoxicity, and immune responses in fish: a review. Environ Toxicol Phar 68:101–108. https://doi.org/10.1016/j.etap.2019.03.010
Liao XD, Ma G, Cai J, Fu Y, Yan XY, Wei XB, Zhang RJ (2015) Effects of Clostridium butyricum on growth performance, antioxidation, and immune function of broilers. Poultry Sci 94:662–667. https://doi.org/10.3382/ps/pev038
Liu B, Ge X, Xie J, Xu P, He Y, Cui Y, Ming J, Zhou Q, Pan L (2012) Effects of anthraquinone extract from Rheum officinale Bail on the physiological responses and HSP70 gene expression of Megalobrama amblycephala under Aeromonas hydrophila infection. Fish Shellfish Immunol 32:1–7. https://doi.org/10.1016/j.fsi.2011.02.015
Liu HS, Fu SL, Zhang SS, Ding MM, Wang AL (2020) Lead induces structural damage, microbiota dysbiosis and cell apoptosis in the intestine of juvenile bighead carp (Hypophthalmichthys nobilis). Aquaculture 528. https://doi.org/10.1016/j.aquaculture.2020.735573
Lu XJ, Chen J, Huang ZA, Zhuang L, Peng LZ, Shi YH (2012) Influence of acute cadmium exposure on the liver proteome of a teleost fish, ayu (Plecoglossus altivelis). Mol Boil Rep 39:2851–2859. https://doi.org/10.1007/s11033-011-1044-3
Macdonald A, Silk L, Schwartz M, CPlayle R (2002) A lead-gill binding model to predict acute lead toxicity to rainbow trout (Oncorhynchus mykiss). Comp Biochem Phys C 133:227–242. https://doi.org/10.1016/S1532-0456(02)00107-2
Madara JL, Nash S, Moore R, Atisook K (1990) Structure and function of the intestinal epithelial barrier in health and disease. Monogr Pathol 306–324. https://pubmed.ncbi.nlm.nih.gov/2406578/
Mani MS, Kabekkodu SP, Joshi MB, Dsouza HS (2019) Ecogenetics of lead toxicity and its influence on risk assessment. Hum Exp Toxicol 38:1031–1059
Marionnet D, Chambras C, Chambras C, Taysse L, Bosgireaud C, Deschaux P (1998) Modulation of drug-metabolizing systems by bacterial endotoxin in carp liver and immune organs. Ecotox Environ Safe 189–194. https://doi.org/10.1177/0960327119851253
Milner JA (2001) A historical perspective on garlic and cancer. J Nutr 131:1027–1031. https://doi.org/10.1177/10.1093/jn/131.3.1027S
Mokni R, Chakar A, Bleiberg-Daniel F, Mahu JL, Walravens PA, Chappuis P, Navarro J, Lemonnier D (1993) Decreased serum levels of nutritional biochemical indices in healthy children with marginally delayed physical growth. Acta Paediatr 82:539–543. https://doi.org/10.1111/j.1651-2227.1993.tb12748.x
Moniruzzaman M, Midday P, Dhara A, Das D, Ghosal I, Mukherjee D, Chakraborty SB (2017) Change in redox state and heat shock protein expression in an Indian major carp Cirrhinus cirrhosus exposed to zinc and lead. J Toxicol Sci 42:731–740. https://doi.org/10.2131/jts.42.731
Mumtaz S, Ali S, Khan R, Shakir HA, Tahir HM, Mumtaz S, Andleeb S (2020) Therapeutic role of garlic and vitamins C and E against toxicity induced by lead on various organs. Environ Sci Pollut R 27:8953–8964. https://doi.org/10.1007/s11356-020-07654-2
Nijveldt RJ, Van NE, Van HDEC, Boelens PG, Van NK, Van LPAM (2001) Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 74:418–425. https://doi.org/10.1093/ajcn/74.4.418
Nynca J, Dietrich MA, Adamek M, Steinhagen D, Bilinska B, Hejmej A, Ciereszko A (2017) Purification, characterization and expression of transferrin from rainbow trout seminal plasma. Comp Biochem Phys B 208:38–46. https://doi.org/10.1016/j.cbpb.2017.04.002
Ozkan-Yilmaz F, Ozluer-Hunt A, Gunduz SG, Berkoz M, Yalin S (2014) Effects of dietary selenium of organic form against lead toxicity on the antioxidant system in Cyprinus carpio. Fish physiol Biochem 40:355–363. https://doi.org/10.1007/s10695-013-9848-9
Park IS, Lee HW, Ryuk JA, Ko BS (2014) Effects of an aqueous extract of dangguijagyagsan on serum lipid levels and blood flow improvement in ovariectomized rats. Evid Based Complementary Altern Med https://doi.org/10.1155/2014/497836
Pashaki A, Zorriehzahra J, Ghasemi M, Sharifrohani M, Hosseini SMD (2018) Effects of dietary Garlic extract on some blood, immunity and growth parameters of common carp fingerlings (Cyprinus carpio). J Aquat Anim Health 4:28–39. https://doi.org/10.29252/ijaah.4.2.28
Pirsaheb M, Azadi NA, Miglietta ML, Sayadi MH, Blahova J, Fathi M, Mansouri B (2019) Toxicological effects of transition metal-doped titanium dioxide nanoparticles on goldfish (Carassius auratus) and common carp (Cyprinus carpio). Chemosphere 215:904–915. https://doi.org/10.1016/j.chemosphere.2018.10.111
Popek W, Dietrich G, Glogowski J, Demska-Zakes K, Drag-Kozak E, Sionkowski J, Luszczek-Trojan E, Epler P, Demianowicz W, Sarosiek B, Kowalski R, Jankun M, Zakes Z, Krol J, Czerniak S, Szczepkowski M (2006) Influence of heavy metals and 4-nonylphenol on reproductive function in fish. Reprod Bio 175–188.
Pu H, Li X, Du Q, Cui H, Xu Y (2017) Research progress in the application of Chinese herbal medicines in aquaculture: a Review. Engineering 3:731–737. https://doi.org/10.1016/J.ENG.2017.03.017
Rainbow PS, Scott AG, Wiggins EA, Jackson RW (1980) Effect of chelating agents on the accumulation of cadmium by the barnacle Semibalanus balanoides, and complexation of soluble Cd, Zn and Cu. Mar Ecol Prog Ser 2:143–152. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.434.9180&rep=rep1&type=pdf
Rajabiesterabadi H, Yousefi M, Hoseini SM (2020) Enhanced haematological and immune responses in common carp Cyprinus carpio fed with olive leaf extract-supplemented diets and subjected to ambient ammonia. Aquacult Nutr 26:763–771. https://doi.org/10.1111/anu.13035
Raudenská M, Smerkova K, Tanhäuserová V, Gumulec J, Hlavna M, Svobodová M, Pacal L, Babula P, Adam V, Eckschlager T, Kizek R, Masarik M (2012) Metallothionein and its role in detoxification of heavy metals and predisposition to diseases. Praktický lékar̆ 92:322–326
Reyes-Becerril M, Angulo C, Estrada N, Murillo Y, Ascencio-Valle F (2014) Dietary administration of microalgae alone or supplemented with Lactobacillus sakei affects immune response and intestinal morphology of Pacific red snapper (Lutjanus peru). Fish Shellfish Immunol 40:208–216. https://doi.org/10.1016/j.fsi.2014.06.032
Rios JL (2011) Chemical constituents and pharmacological properties of Poria cocos. Planta Med 77:681–691. https://doi.org/10.1055/s-0030-1270823
Rogers JT, Wood CM (2004) Characterization of branchial lead-calcium interaction in the freshwater rainbow trout Oncorhynchus mykiss. J Exp Boil 207:813–825. https://doi.org/10.1242/jeb.00826
Sabolic I (2006) Common mechanisms in nephropathy induced by toxic metals. Nephron Physiol 104:107–114. https://doi.org/10.1159/000095539
Sassi A, Darias MJ, Said K, Messaoudi I, Gisbert E (2013) Cadmium exposure affects the expression of genes involved in skeletogenesis and stress response in gilthead sea bream larvae. Fish Physiol Biochem 39:649–659. https://doi.org/10.1007/s10695-012-9727-9
Sharma V, Sharma A, Kansal L (2010) The effect of oral administration of Allium sativum extracts on lead nitrate induced toxicity in male mice. Food Chem Toxicol 48:928–936. https://doi.org/10.1016/j.fct.2010.01.002
Singh N, Kumar A, Gupta VK, Sharma B (2018) Biochemical and molecular bases of Lead-induced toxicity in mammalian systems and possible mitigations. Chem Res Toxicol 31:1009–1021. https://doi.org/10.1021/acs.chemrestox.8b00193
Smith AM, Zeve DR, Grisel JJ, Chen WJA (2005) Neonatal alcohol exposure increases malondialdehyde (MDA) and glutathione (GSH) levels in the developing cerebellum. Dev Brain Res 160:231–238. https://doi.org/10.1016/j.devbrainres.2005.09.004
Srikanth K, Pereira E, Duarte AC, Ahmad I (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish-a review. Environ Sci Pollut R 20:2133–2149. https://doi.org/10.1007/s11356-012-1459-y
Sun ZZ, Tan XH, Ye HQ, Zou CY, Ye CX, Wang AL (2018) Effects of dietary Panax notoginseng extract on growth performance, fish composition, immune responses, intestinal histology and immune related genes expression of hybrid grouper (Epinephelus lanceolatus male X Epinephelus fuscoguttatus female) fed high lipid diets. Fish Shellfish Immunol 73:234–244. https://doi.org/10.1016/j.fsi.2017.11.007
Tan XH, Sun ZZ, Huang Z, Zhou CP, Lin HZ, Tan LJ, Xun PW, Huang Q (2017) Effects of dietary hawthorn extract on growth performance, immune responses, growth- and immune-related genes expression of juvenile golden pompano (Trachinotus ovatus) and its susceptibility to Vibrio harveyi infection. Fish Shellfish Immunol 70:656–664. https://doi.org/10.1016/j.fsi.2017.09.041
Tan XH, Sun ZZ, Zhou CP, Huang Z, Tan LJ, Xun PW, Huang QQ, Lin HZ, Ye CX, Wang AL (2018) Effects of dietary dandelion extract on intestinal morphology, antioxidant status, immune function and physical barrier function of juvenile golden pompano Trachinotus ovatus. Fish Shellfish Immunol 73:197–206. https://doi.org/10.1016/j.fsi.2017.12.020
Tang L, Xiong ZY, Zhang YQ (2008) Effects of Pueraria Flavonid on expression of transferrin receptor in quadriceps of exercise-training rats. Food Sci 29:412–415
Tian H, Liu Z, Pu Y, Bao Y (2019) Immunomodulatory effects exerted by Poria Cocos polysaccharides via TLR4/TRAF6/NF-κB signaling in vitro and in vivo. Biomed Pharmacother 112:108709. https://doi.org/10.1016/j.biopha.2019.108709
Tian LX, Liu YJ, Yang HJ, Liang GY, Niu J (2012) Effects of different dietary wheat starch levels on growth, feed efficiency and digestibility in grass carp (Ctenopharyngodon idella). Aquacult Int 20:283–293. https://doi.org/10.1007/s10499-011-9456-6
Tjälve H, Gottofrey J (1991) Effects of lipophilic complex formation on the uptake and distribution of some metals in fish. Pharmacol Toxicol 68:430–439. https://doi.org/10.1111/j.1600-0773.1991.tb01266.x
Torrecillas S, Montero D, Caballero MJ, Robaina L, Zamorano MJ, Sweetman J, Izquierdo M (2015) Effects of dietary concentrated mannan oligosaccharides supplementation on growth, gut mucosal immune system and liver lipid metabolism of European sea bass (Dicentrarchus labrax) juveniles. Fish Shellfish Immunol 42:508–516. https://doi.org/10.1016/j.fsi.2014.11.033
Wang Y, Wimmer U, Lichtlen P, Inderbitzin D (2004) Metal-responsive transcription factor-1 (MTF-1) is essential for embryonic liver development and heavy metal detoxification in the adult liver. Faseb J 18:1071–1079. https://doi.org/10.1096/fj.03-1282com
Wang YZ, Li T, Zhao YL, Zhang J, Liu HG (2012) Contents of some metabolites in the peel and flesh of the medicinal mushroom Wolfiporia cocos (F.A. Wolf) Ryvarden et Gilb. (Higher Basidiomycetes). Int J Med Mushrooms 14:79–83. https://doi.org/10.1615/IntJMedMushr.v14.i1.80
Yin YW, Zhang PJ, Yue XY, Du XY, Li W, Yin YL, Yi C, Li YH (2018) Effect of sub-chronic exposure to lead (Pb) and Bacillus subtilis on Carassius auratus gibelio: Bioaccumulation, antioxidant responses and immune responses. Ecotox Environ Safe 161:755–762. https://doi.org/10.1016/j.ecoenv.2018.06.056
Yousefi M, Vatnikov YA, Kulikov EV, Plushikov VG, Drukovsky SG, Hoseinifar SH, Doan HV (2020) The protective effects of dietary garlic on common carp (Cyprinus carpio) exposed to ambient ammonia toxicity. Aquaculture 526. https://doi.org/10.1016/j.aquaculture.2020.735400
Zakes Z, Kowalska A, Demska-Zakes K, Jeney G, Jeney Z (2008) Effect of two medicinal herbs (Astragalus radix and Lonicera japonica) on the growth performance and body composition of juvenile pikeperch [Sander lucioperca (L.)]. Aquac Res 39:1149–1160. https://doi.org/10.1111/j.1365-2109.2008.01977.x
Zhai QX, Liu Y, Wang C, Qu DW, Zhao JX, Zhang H, Tian FW, Chen W (2019) Lactobacillus plantarum CCFM8661 modulates bile acid enterohepatic circulation and increases lead excretion in mice. Food Funct 10:1455–1464. https://doi.org/10.1039/c8fo02554a
Zhai QX, Wang HC, Tian FW, Zhao JX, Zhang H, Chen W (2017) Dietary Lactobacillus plantarum supplementation decreases tissue lead accumulation and alleviates lead toxicity in Nile tilapia (Oreochromis niloticus). Aquac Res 48:5094–5103. https://doi.org/10.1111/are.13326
Zhou C, Lin H, Ge X, Niu J, Wang J, Wang Y, Chen L, Huang Z, Yu W, Tan X (2015) The effects of dietary soybean isoflavones on growth, innate immune responses, hepatic antioxidant abilities and disease resistance of juvenile golden pompano Trachinotus ovatus. Fish shellfish immunol 43:158–166. https://doi.org/10.1016/j.fsi.2014.12.014
Zhou F, Zhou J, Shao QJ, Wang Y, Li H, Gao S, Hua Y (2012) Effects of arginine-deficient and replete diets on growth performance, digestive enzyme activities and genes expression of black sea bream, Acanthopagrus schlegelii, juveniles. J World Aquacult Soc 43:828–839. https://doi.org/10.1111/j.1749-7345.2012.00606.x
Acknowledgements
This project was supported by Guangzhou Science and Technology Program Key projects (201804020058), Natural Science Foundation of Guangdong Province, China (2020A1515111121), Guangdong Provincial Key Laboratory for Healthy and Safe Aquaculture, South China Normal University (GDKLHSA1902).
Author contributions
Writing—review & editing, investigation, visualization: HL; investigation, writing—review & editing: SZ; investigation: Qiu Ming; writing—review & editing, resources: AW; writing—review & editing: JY; conceptualization, writing—review & editing, investigation, resources: SF.
Funding
This project was supported by Guangzhou Science and Technology Program Key projects (Grant numbers: 201804020058), Natural Science Foundation of Guangdong Province, China (Grant numbers: 2020A1515111121), Guangdong Provincial Key Laboratory for Healthy and Safe Aquaculture, South China Normal University (Grant numbers: GDKLHSA1902).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
This article does not contain any studies with human participants performed by any of the authors. All animal experimental procedures were carried out in accordance with the Regulations for Animal Experimentation of South China Normal University (SCNU-SLS-2020-001), and the animal facility was based on the National Institutes of Health guide for the care and use of Laboratory Animals (NIH Publications No. 8023).
Informed consent
Informed consent was not required, as this research did not require human participants, their data or biological material. Additionally, all information is anonymized and the submission does not include images that may identify any people.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Liu, H., Zhang, S., Qiu, M. et al. Garlic (Allium sativum) and Fu-ling (Poria cocos) mitigate lead toxicity by improving antioxidant defense mechanisms and chelating ability in the liver of grass carp (Ctenopharyngodon idella). Ecotoxicology 30, 885–898 (2021). https://doi.org/10.1007/s10646-021-02405-6
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-021-02405-6