Abstract
The cadmium (Cd) is considered one of the widespread toxic metals in the aquatic and terrestrial environments, which is due to its long half-life, non-degradable characteristic, and toxicity. Aqueous extract of freeze-dried Moringa oleifera (Moringaceae family) leaves was examined for protective effect and antioxidant power against Cd toxicity. The results revealed that Moringa aqueous extract (MAE) has contents of total polyphenols and flavonoids about 30.14 mg GAE/g and 18.35 mg QE/g respectively. Furthermore, phenolic compounds in leaves of Moringa were studied using a high-performance liquid chromatography coupled with mass spectrometry (HPLC-MS). Results showed that the largest number of phenolic compounds determined in leaves of Moringa belongs to flavonoids. Moreover, biological properties were determined by radical scavenging capacity (DPPH) and ferric-reducing power (FRAP). Cytoprotective effect and antioxidant power of Moringa extract were assessed using the mitochondrial activity testing method (MTT test), malondialdehyde (MDA), and reactive oxygen species (ROS) production. Results indicate that Moringa aqueous extract have a significant (i) proliferative, (ii) antioxidant, and (iii) cytoprotective effect on HCT116 and HEK293 cells against metal toxicity.
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References
Abdeen A, Ghonim A, El-Shawarby R et al (2017) Protective effect of cinnamon against cadmium-induced hepatorenal oxidative damage in rats. Int J Pharmacol Toxicol 5:17. https://doi.org/10.14419/ijpt.v5i1.7119
Abdeen A, Abou-Zaid OA, Abdel-Maksoud HA, Aboubakr M, Abdelkader A, Abdelnaby A, Abo-Ahmed AI, el-Mleeh A, Mostafa O, Abdel-Daim M, Aleya L (2019) Cadmium overload modulates piroxicam-regulated oxidative damage and apoptotic pathways. Environ Sci Pollut Res 26:25167–25177. https://doi.org/10.1007/s11356-019-05783-x
Akinyemi AJ, Onyebueke N, Faboya OA, Onikanni SA, Fadaka A, Olayide I (2017) Curcumin inhibits adenosine deaminase and arginase activities in cadmium-induced renal toxicity in rat kidney. J Food Drug Anal 25:438–446. https://doi.org/10.1016/J.JFDA.2016.06.004
Al_husnan LA, Alkahtani MDF (2016) Impact of Moringa aqueous extract on pathogenic bacteria and fungi in vitro. Ann Agric Sci 61:247–250. https://doi.org/10.1016/J.AOAS.2016.06.003
Alschuler L (1998) Green tea: healing tonic. Am J Natur Med 5:28–31
Amaglo NK, Bennett RN, Lo Curto RB et al (2010) Profiling selected phytochemicals and nutrients in different tissues of the multipurpose tree Moringa oleifera L., grown in Ghana. Food Chem 122:1047–1054. https://doi.org/10.1016/J.FOODCHEM.2010.03.073
American Society of Enologists. K, Singleton VL (1977) American Journal of Enology and Viticulture. American Society of Enologists
Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res 22:17022–17030. https://doi.org/10.1007/s11356-015-4882-z
Balakrishnan BB, Krishnasamy K, Mayakrishnan V, Selvaraj A (2019) Moringa concanensis Nimmo extracts ameliorates hyperglycemia-mediated oxidative stress and upregulates PPARγ and GLUT4 gene expression in liver and pancreas of streptozotocin-nicotinamide induced diabetic rats. Biomed Pharmacother 112:108688. https://doi.org/10.1016/J.BIOPHA.2019.108688
Banerjee S, Flores-Rozas H (2005) Cadmium inhibits mismatch repair by blocking the ATPase activity of the MSH2-MSH6 complex. Nucleic Acids Res 33:1410–1419. https://doi.org/10.1093/nar/gki291
Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76. https://doi.org/10.1006/ABIO.1996.0292
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 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
Castro-López C, Ventura-Sobrevilla JM, González-Hernández MD, Rojas R, Ascacio-Valdés JA, Aguilar CN, Martínez-Ávila GCG (2017) Impact of extraction techniques on antioxidant capacities and phytochemical composition of polyphenol-rich extracts. Food Chem 237:1139–1148. https://doi.org/10.1016/J.FOODCHEM.2017.06.032
Chang CC, Yang MH, Wen HM et al (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. 10:178–182
Chen AY, Chen YC (2013) A review of the dietary flavonoid, kaempferol on human health and cancer chemoprevention. Food Chem 138:2099–2107. https://doi.org/10.1016/J.FOODCHEM.2012.11.139
Connor WE (2000) Importance of n−3 fatty acids in health and disease. Am J Clin Nutr 71:171S–175S. https://doi.org/10.1093/ajcn/71.1.171S
Coppin JP, Xu Y, Chen H et al (2013) Determination of flavonoids by LC/MS and anti-inflammatory activity in Moringa oleifera. J Funct Foods 5:1892–1899. https://doi.org/10.1016/J.JFF.2013.09.010
Coz-Bolaños X, Campos-Vega R, Reynoso-Camacho R et al (2018) Moringa infusion (Moringa oleifera) rich in phenolic compounds and high antioxidant capacity attenuate nitric oxide pro-inflammatory mediator in vitro. Ind Crop Prod 118:95–101. https://doi.org/10.1016/J.INDCROP.2018.03.028
Foidl N, Tanzania) P de D des P de M fre 29 O-2 N 2001 D es S (United R of, Makkar HPS, Becker K (2001) Potentiel de Moringa oleifera en agriculture et dans l’industrie
Horiguchi H, Harada A, Oguma E et al (2000) Cadmium-induced acute hepatic injury is exacerbated in human interleukin-8 transgenic mice. Toxicol Appl Pharmacol 163:231–239. https://doi.org/10.1006/TAAP.1999.8877
Jimoh TO, Jimoh TO (2018) Enzymes inhibitory and radical scavenging potentials of two selected tropical vegetable (Moringa oleifera and Telfairia occidentalis) leaves relevant to type 2 diabetes mellitus. Rev Bras Farmacogn 28:73–79. https://doi.org/10.1016/j.bjp.2017.04.003
Kalidindi N, Thimmaiah NV, Jagadeesh NV, Nandeep R, Swetha S, Kalidindi B (2015) Antifungal and antioxidant activities of organic and aqueous extracts of Annona squamosa Linn. leaves. J Food Drug Anal 23:795–802. https://doi.org/10.1016/J.JFDA.2015.04.012
Kandeil MA, Mohammed ET, Hashem KS et al (2019) Moringa seed extract alleviates titanium oxide nanoparticles (TiO2-NPs)-induced cerebral oxidative damage , and increases cerebral mitochondrial viability. Environ Sci Pollut Res 1–16. https://doi.org/10.1007/s11356-019-05514-2
Karthivashan G, Tangestani Fard M, Arulselvan P, Abas F, Fakurazi S (2013) Identification of bioactive candidate compounds responsible for oxidative challenge from hydro-ethanolic extract of Moringa oleifera leaves. J Food Sci 78:C1368–C1375. https://doi.org/10.1111/1750-3841.12233
Kashiwada Y, Ahmed FA, Kurimoto S, Kim SY, Shibata H, Fujioka T, Takaishi Y (2012) New α-glucosides of caffeoyl quinic acid from the leaves of Moringa oleifera lam. J Nat Med 66:217–221. https://doi.org/10.1007/s11418-011-0563-5
Kiehne A, Engelhardt UH (1996) Thermospray-LC-MS analysis of various groups of polyphenols in tea: I. Catechins, flavonol O-glycosides and flavone C-glycosides. Zeitschrift fur Leb -Untersuchung und -forsch 202:48–54. https://doi.org/10.1007/BF01229684
Lin J-T, Liu S-C, Kuo L-C, Yang D-J (2018) Composition of phenolic compounds and antioxidant attributes of Cyclea gracillima Diels extracts. J Food Drug Anal 26:193–200. https://doi.org/10.1016/J.JFDA.2017.03.004
Liu L, Zhu B, Wang GX (2015) Azoxystrobin-induced excessive reactive oxygen species (ROS) production and inhibition of photosynthesis in the unicellular green algae Chlorella vulgaris. Environ Sci Pollut Res 22:7766–7775. https://doi.org/10.1007/s11356-015-4121-7
Meir S, Kanner J, Akiri B, Philosoph-Hadas S (1995) Determination and involvement of aqueous reducing compounds in oxidative defense systems of various senescing leaves. J Agric Food Chem 43:1813–1819. https://doi.org/10.1021/jf00055a012
Mousa AA, El-Gansh HAI, Eldaim MAA et al (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 26:32488–32504. https://doi.org/10.1007/s11356-019-06368-4
Raza H, John A, Benedict S (2011) Acetylsalicylic acid-induced oxidative stress, cell cycle arrest, apoptosis and mitochondrial dysfunction in human hepatoma HepG2 cells. Eur J Pharmacol 668:15–24. https://doi.org/10.1016/j.ejphar.2011.06.016
Rocha MI, Rodrigues MJ, Pereira C et al (2017) Biochemical profile and in vitro neuroprotective properties of Carpobrotus edulis L., a medicinal and edible halophyte native to the coast of South Africa. South African J Bot 111:222–231. https://doi.org/10.1016/J.SAJB.2017.03.036
Rodríguez-Pérez C, Quirantes-Piné R, Cutiérrez-Fernández A et al (2015) Optimization of extraction method to obtain a phenolic compounds-rich extract from Moringa oleifera Lam leaves. Ind Crop Prod 66:246–254. https://doi.org/10.1016/j.indcrop.2015.01.002
Shaw JR, Colbourne JK, Davey JC, Glaholt SP, Hampton TH, Chen CY, Folt CL, Hamilton JW (2007) Gene response profiles for Daphnia pulex exposed to the environmental stressor cadmium reveals novel crustacean metallothioneins. BMC Genomics 8:477. https://doi.org/10.1186/1471-2164-8-477
Soares SS, Martins H, Gutiérrez-Merino C, Aureliano M (2008) Vanadium and cadmium in vivo effects in teleost cardiac muscle: metal accumulation and oxidative stress markers. Comp Biochem Physiol Part C Toxicol Pharmacol 147:168–178. https://doi.org/10.1016/J.CBPC.2007.09.003
Souid-Mensi G, Moukha S, Mobio TA, Maaroufi K, Creppy EE (2008) The cytotoxicity and genotoxicity of okadaic acid are cell-line dependent. Toxicon 51:1338–1344. https://doi.org/10.1016/J.TOXICON.2008.03.002
Štork F, Bačkor M, Klejdus B, Hedbavny J, Kováčik J (2013) Changes of metal-induced toxicity by H2O2/NO modulators in Scenedesmus quadricauda (Chlorophyceae). Environ Sci Pollut Res 20:5502–5511. https://doi.org/10.1007/s11356-013-1541-0
Susin SA, Zamzami N, Kroemer G (1998) Mitochondria as regulators of apoptosis: doubt no more. Biochim Biophys Acta Bioenerg 1366:151–165. https://doi.org/10.1016/S0005-2728(98)00110-8
Terao J, Piskula MK (1999) Flavonoids and membrane lipid peroxidation inhibition. Nutrition 15:790–791. https://doi.org/10.1016/s0899-9007(99)00159-8
Tesfay SZ, Magwaza LS, Mbili N, Mditshwa A (2017) Carboxyl methylcellulose (CMC) containing moringa plant extracts as new postharvest organic edible coating for avocado (Persea americana Mill.) fruit. Sci Hortic (Amsterdam) 226:201–207. https://doi.org/10.1016/J.SCIENTA.2017.08.047
Tiloke C, Anand K, Gengan RM, Chuturgoon AA (2018) Moringa oleifera and their phytonanoparticles: potential antiproliferative agents against cancer. Biomed Pharmacother 108:457–466. https://doi.org/10.1016/J.BIOPHA.2018.09.060
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The authors would like to acknowledge Prof. Fethia Harzallah-Skhiri, Director of the High Institute of Biotechnology of Monastir, Tunisia, for botanical identification of the plant material.
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Souid, G., Sfar, M., Timoumi, R. et al. Protective effect assessment of Moringa oleifera against cadmium-induced toxicity in HCT116 and HEK293 cell lines. Environ Sci Pollut Res 27, 23783–23792 (2020). https://doi.org/10.1007/s11356-020-08730-3
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DOI: https://doi.org/10.1007/s11356-020-08730-3