Abstract
Lead (Pb) is an environmental toxicant; its consumption can induce renal deficits. In this study, we explored the possible protective efficiency of Moringa oleifera extract (MOE) against lead acetate (PbAc)-mediated reprotoxicity. Four experimental groups of seven rats each were used: control, PbAc, MOE, and MOE+PbAc groups. All groups were given their respective treatment for 4 weeks. PbAc impaired the oxidative/antioxidative balance in the renal tissue, as shown by the decreased antioxidant proteins (glutathione, glutathione reductase, glutathione peroxidase, catalase, and superoxide dismutase) and increased oxidants (lipid peroxidation and nitric oxide). Additionally, PbAc enhanced the progression of kidney inflammation by increasing tumor necrosis factor-alpha, interleukin-1 beta, and nuclear factor kappa B associated with upregulation of inducible nitric oxide synthase. Moreover, a dysregulation in the apoptotic-regulating proteins (Bax, caspase-3, and Bcl2) were recorded upon PbAc exposure. Remarkably, MOE oral administration restored redox homeostasis, suppressed the inflammatory and apoptotic responses in the kidney tissue. Our findings point out that MOE could be used as an alternative remedy to overcome the adverse effects of Pb exposure, which may be due to its potent antioxidant, anti-inflammatory, and anti-apoptotic effects.
Similar content being viewed by others
References
Abdel Moneim AE (2012) Flaxseed oil as a neuroprotective agent on lead acetate-induced monoamineric alterations and neurotoxicity in rats. Biol Trace Element Res 148:363–370. https://doi.org/10.1007/s12011-012-9370-4
Abd-Elhakim YM, El Bohi KM, Hassan SK, El Sayed S, Abd-Elmotal SM (2018) Palliative effects of Moringa olifera ethanolic extract on hemato-immunologic impacts of melamine in rats. Food Chem Toxicol 114:1–10. https://doi.org/10.1016/j.fct.2018.02.020
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Aju BY, Rajalakshmi R, Mini S (2019) Protective role of Moringa oleifera leaf extract on cardiac antioxidant status and lipid peroxidation in streptozotocin induced diabetic rats. Heliyon 5:e02935. https://doi.org/10.1016/j.heliyon.2019.e02935
Albasher G, Albrahim T, Alsultan N, Alfaraj S, Alharthi MS, Kassab RB, Abdel Moneim AE (2019a) Red beetroot extract mitigates chlorpyrifos-induced reprotoxicity associated with oxidative stress, inflammation, and apoptosis in rats. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-019-07009-6
Albasher G, Albrahim T, Alsultan N, Alfaraj S, Alharthi MS, Kassab RB, Moneim AEA (2019b) Red beetroot extract mitigates chlorpyrifos-induced reprotoxicity associated with oxidative stress, inflammation, and apoptosis in rats. Environ Sci Pollut Res:1–13
Al-Megrin WA et al (2019) Antagonistic efficacy of Luteolin against Lead acetate exposure-associated with hepatotoxicity is mediated via antioxidant, anti-inflammatory, and anti-apoptotic activities antioxidants (Basel) 9. https://doi.org/10.3390/antiox9010010
AL-Megrin WA, Soliman D, Kassab RB, Metwally DM, Abdel Moneim AE, El-Khadragy MF (2020) Coenzyme Q10 activates the antioxidant machinery and inhibits the inflammatory and apoptotic cascades against lead acetate-induced renal injury in rats. Front Physiol 11. https://doi.org/10.3389/fphys.2020.00064
Arevalo-Hijar L, Aguilar-Luis MA, Caballero-Garcia S, Gonzales-Soto N, Del Valle-Mendoza J (2018) Antibacterial and cytotoxic effects of Moringa oleifera (moringa) and Azadirachta indica (neem) methanolic extracts against strains of Enterococcus faecalis. Int J Dentist 2018:1071676 doi:https://doi.org/10.1155/2018/1071676, , 5
Baty RS, Hassan KE, Alsharif KF, El-Hennamy RE, Elmahallawy EK, Hafez MM, Moneim AA, Kassab RB (2020) Neuroprotective role of luteolin against lead acetate-induced cortical damage in rats. Hum Exp Toxicol. https://doi.org/10.1177/0960327120913094
Bhattacharya A, Tiwari P, Sahu PK, Kumar S (2018) A review of the phytochemical and pharmacological characteristics of Moringa oleifera. J Pharm Bioall Sci 10:181–191. https://doi.org/10.4103/JPBS.JPBS_126_18
De Vega L, Fernandez RP, Mateo MC, Bustamante JB, Herrero AM, Munguira EB (2002) Glutathione determination and a study of the activity of glutathione-peroxidase, glutathione-transferase, and glutathione-reductase in renal transplants. Ren Fail 24:421–432
Dkhil MA, Al-Khalifa MS, Al-Quraishy S, Zrieq R, Abdel Moneim AE (2016) Indigofera oblongifolia mitigates lead-acetate-induced kidney damage and apoptosis in a rat model drug design, development and therapy 10:1847-1856. https://doi.org/10.2147/DDDT.S105511
Edeogu CO, Kalu ME, Famurewa AC, Asogwa NT, Onyeji GN, Ikpemo KO (2019) Nephroprotective effect of moringa oleifera seed oil on gentamicin-induced nephrotoxicity in rats: biochemical evaluation of antioxidant, anti-inflammatory, and antiapoptotic pathways. J Am Coll Nutr:1-9 https://doi.org/10.1080/07315724.2019.1649218
El Shanawany EE, Fouad EA, Keshta HG, Hassan SE, Hegazi AG, Abdel-Rahman EH (2019) Immunomodulatory effects of Moringa oleifera leaves aqueous extract in sheep naturally co-infected with Fasciola gigantica and Clostridium novyi. J Parasit Dis 43:583–591. https://doi.org/10.1007/s12639-019-01130-6
Elblehi SS, El Euony OI, El-Nahas AF (2019) Partial ameliorative effect of Moringa leaf ethanolic extract on the reproductive toxicity and the expression of steroidogenic genes induced by subchronic cadmium in male rats. Environ Sci Pollut Res Int 26:23306–23318. https://doi.org/10.1007/s11356-019-05607-y
El-Hadary AE, Ramadan MF (2019) Antioxidant traits and protective impact of Moringa oleifera leaf extract against diclofenac sodium-induced liver toxicity in rats. J Food Biochem 43:e12704. https://doi.org/10.1111/jfbc.12704
Elkhadragy MF et al (2018) Protective effects of Fragaria ananassa methanolic extract in a rat model of cadmium chloride-induced neurotoxicity. Biosci Rep. https://doi.org/10.1042/BSR20180861
El-Khadragy M et al (2018) Clinical efficacy associated with enhanced antioxidant enzyme activities of silver nanoparticles biosynthesized using Moringa oleifera leaf extract, against cutaneous leishmaniasis in a murine model of Leishmania major. Int J Environ Res Public Health 15. https://doi.org/10.3390/ijerph15051037
Ellman GL, Courtney KD, Andres V Jr, Feather-stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Fahey JW, Wade KL, Stephenson KK, Shi Y, Liu H, Panjwani AA, Warrick CR, Olson ME (2019) A strategy to deliver precise oral doses of the glucosinolates or isothiocyanates from Moringa oleifera leaves for use in clinical studies. Nutrients 11: https://doi.org/10.3390/nu11071547
Farag I, Roshdy H, Radwan H, Ghaly I, Salah S, Abdel-Rahim E, Abdalla A (2018) Ameliorative role of ethanolic extract of Moringa oleifera leaf on aflatoxin B1-induced genotoxicity and biochemical alterations in rats. J Arab Soc Med Res 13:60–70. https://doi.org/10.4103/jasmr.jasmr_33_17
Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131–138
Mallya R, Chatterjee PK, Vinodini NA, Chatterjee P, Mithra P (2017) Moringa oleifera leaf extract: beneficial effects on cadmium induced toxicities - a review. J Clin Diagn Res 11:CE01–CE04. https://doi.org/10.7860/JCDR/2017/21796.9671
Mansour HH, El Azeem MGA, Ismael NE (2014) Protective effect of Moringa oleifera on γ-radiation-induced hepatotoxicity and nephrotoxicity in rats. AJPCT 2:495–508
Mehta A, Agrawal B (2008) Investigation into the mechanism of action of Moringa oleifera for its anti-asthmatic activity. Orient Pharm Exp Med 8:24–31
Minaiyan M, Asghari G, Taheri D, Saeidi M, Nasr-Esfahani S (2014) Anti-inflammatory effect of Moringa oleifera Lam. seeds on acetic acid-induced acute colitis in rats. Avicenna J Phytomed 4:127–136
Mitra P, Sharma S, Purohit P, Sharma P (2017) Clinical and molecular aspects of lead toxicity: an update. Crit Rev Clin Lab Sci 54:506–528. https://doi.org/10.1080/10408363.2017.1408562
Moneim AEA (2016) Indigofera oblongifolia prevents lead acetate-induced hepatotoxicity, oxidative stress, fibrosis and apoptosis in rats. PLoS One 11:e0158965
Mousa AA, El-Gansh HAI, Eldaim MAA, Mohamed MAE, Morsi AH, El Sabagh HS (2019) Protective effect of Moringa oleifera leaves ethanolic extract against thioacetamide-induced hepatotoxicity in rats via modulation of cellular antioxidant, apoptotic and inflammatory markers. Environ Sci Pollut Res Int 26:32488–32504. https://doi.org/10.1007/s11356-019-06368-4
Nafiu AO, Akomolafe RO, Alabi QK, Idowu CO, Odujoko OO (2019) Effect of fatty acids from ethanol extract of Moringa oleifera seeds on kidney function impairment and oxidative stress induced by gentamicin in rats. Biomed Pharmacother 117:109154. https://doi.org/10.1016/j.biopha.2019.109154
Nishikimi M, Appaji N, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46:849–854
Obembe OO, Raji Y (2018) Effects of aqueous extract of Moringa oleifera seed on cadmium-induced reproductive toxicity in male Wistar rats. Afr Health Sci 18:653–663. https://doi.org/10.4314/ahs.v18i3.23
Oguntibeju OO, Aboua GY, Omodanisi EI (2019) Effects of Moringa oleifera on oxidative stress, apoptotic and inflammatory biomarkers in streptozotocin-induced diabetic animal model. S Afr J Bot. https://doi.org/10.1016/j.sajb.2019.08.039
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169
Singh BN, Singh BR, Singh RL, Prakash D, Dhakarey R, Upadhyay G, Singh HB (2009) Oxidative DNA damage protective activity, antioxidant and anti-quorum sensing potentials of Moringa oleifera. Food Chem Toxicol 47:1109–1116. https://doi.org/10.1016/j.fct.2009.01.034
Sudjarwo SA, Eraiko K, Sudjarwo GW, Koerniasari (2017) Protective effects of piperine on lead acetate induced-nephrotoxicity in rats. Iranian J Basic Med Sci 20:1227–1231. https://doi.org/10.22038/IJBMS.2017.9487
Velaga MK, Daughtry LK, Jones AC, Yallapragada PR, Rajanna S, Rajanna B (2014) Attenuation of lead-induced oxidative stress in rat brain, liver, kidney and blood of male Wistar rats by Moringa oleifera seed powder. J Environ Pathol Toxicol Oncol:323–337. https://doi.org/10.1615/jenvironpatholtoxicoloncol.2014011656
Xu J, Lian LJ, Wu C, Wang XF, Fu WY, Xu LH (2008) Lead induces oxidative stress, DNA damage and alteration of p53, Bax and Bcl-2 expressions in mice. Food Chem Toxicol 46:1488–1494. https://doi.org/10.1016/j.fct.2007.12.016
Yin M et al (2019) Oleuropein suppresses oxidative, inflammatory, and apoptotic responses following glycerol-induced acute kidney injury in rats. Life Sci 232:116634. https://doi.org/10.1016/j.lfs.2019.116634
Yousef S, Omar A, Fahad A, Abdel Moneim AE, Metwally DM, El-khadragy MF, Kassab RB (2019) The neuroprotective role of coenzyme Q10 against lead acetate-induced neurotoxicity is mediated by antioxidant, anti-inflammatory and anti-apoptotic activities. Int J Environ Res Public Health 16:2895
Zeng K et al (2019) Moringa oleifera seed extract protects against brain damage in both the acute and delayed stages of ischemic stroke. Exp Gerontol 122:99–108. https://doi.org/10.1016/j.exger.2019.04.014
Zhang H, Shang C, Tian Z, Amin HK, Kassab RB, Abdel Moneim AE, Zhang Y (2020) Diallyl disulfide suppresses inflammatory and oxidative machineries following carrageenan injection-induced paw edema in mice. Mediat Inflamm 2020:8508906. https://doi.org/10.1155/2020/8508906
Acknowledgments
The authors would like to extend their sincere appreciation to the Research Supporting Project number: RSP-2020/95, King Saud University, Riyadh, Saudi Arabia.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Lotfi Aleya
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
Abdel-Daim, M.M., Alkahtani, S., Almeer, R. et al. Alleviation of lead acetate-induced nephrotoxicity by Moringa oleifera extract in rats: highlighting the antioxidant, anti-inflammatory, and anti-apoptotic activities. Environ Sci Pollut Res 27, 33723–33731 (2020). https://doi.org/10.1007/s11356-020-09643-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-09643-x