Ameliorative effect of water spinach, Ipomea aquatica (Convolvulaceae), against experimentally induced arsenic toxicity

Journal of Translational Medicine

Vincenzo De Feo¹  Muhammad Zia-Ul-Haq³  Ritu Khanra²  Moumita Gangopadhyay⁴  Saikat Dewanjee²  Tarun K Dua² 

[1] Department of Pharmacy, University of Salerno, Fisciano, Salerno 84084, Italy;Advanced Pharmacognosy Research Laboratory, Department of Pharmaceutical Technology, Jadavpur University, Kolkata 700032, India;The Patent Office, Karachi 74470, Pakistan;Biophysics Division, Saha Institute of Nuclear Physics, Kolkata 700064, India

关键词: Oxidative stress;    NaAsO2;    Ipomea aquatica;    As toxicity;    Apoptosis;   

Others  :  1137563
DOI  :  10.1186/s12967-015-0430-3

 received in 2015-01-16, accepted in 2015-02-06,  发布年份 2015

【 摘 要 】

Background

Ipomea aquatica (Convolvulaceae) is traditionally used against Arsenic (As) poisoning in folk medicines in India. The present study was designed to explore the therapeutic role of aqueous extract of I. aquatica (AEIA) against As-intoxication.

Methods

AEIA was chemically standardized by spectroscopic and chromatographic analysis. The cytoprotective role of AEIA was measured on isolated murine hepatocytes. The effect on redox status were measured after incubating the hepatocytes with NaAsO₂ (10 μM) + AEIA (400 μg/ml). The protective effect of AEIA (400 μg/ml) in expressions of apoptotic proteins were estimated in vitro. The protective role of AEIA was measured by in vivo assay in mice. Haematological, biochemical, As bioaccumulation and histological parameters were evaluated to ensure the protective role of AEIA (100 mg/kg) against NaAsO₂ (10 mg/kg) intoxication.

Results

Phytochemical analysis revealed presence of substantial quantities of phenolics, flavonoids, saponins and ascorbic acid in AEIA. Incubation of murine hepatocytes with AEIA (0–400 μg/ml) + NaAsO₂ (10 μM) exerted a concentration dependent cytoprotective effect. Incubation of murine hepatocytes with NaAsO₂ (10 μM, ~ IC₅₀) induced apoptosis via augmenting oxidative stress. NaAsO₂ treated hepatocytes exhibited significantly (p < 0.01) enhanced levels of ROS production, lipid peroxidation and protein carbonylation with concomitant depletion of antioxidant enzymes (p < 0.05-0.01) and GSH (p < 0.01) levels. However, AEIA (400 μg/ml) + NaAsO₂ (10 μM) could significantly (p < 0.05-0.01) reinstate the aforementioned parameters to near-normal status. Besides, AEIA (400 μg/ml) could significantly counteract (p <0.05-0.01) ROS mediated alteration in the expressions of apoptotic proteins viz. Bcl-2, BAD, Cyt C, Apaf 1, caspases, Fas and Bid. In in vivo bioassay, NaAsO₂ (10 mg/kg) treatment in mice caused significantly (p < 0.05-0.01) elevated As bioaccumulation, ATP levels, DNA fragmentations and oxidative stress in the liver, kidney, heart, brain and testes along with alteration in cytoarchitecture of these organs. In addition, the serum biochemical and haematological parameters were significantly (p < 0.05-0.01) altered in the NaAsO₂-treated animals. However, concurrent administration of AEIA (100 mg/ml) could significantly reinstate the NaAsO₂-induced pathogenesis.

Conclusion

Presence of substantial quantities of dietary antioxidants within AEIA would be responsible for overall protective effect.

【 授权许可】

   
2015 Dua et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】

• [1]Das AK, Sahu R, Dua TK, Bag S, Gangopadhyay M, Sinha MK, et al.: Arsenic-induced myocardial injury: Protective role of Corchorus olitorius leaves. Food Chem Toxicol 2010, 48:1210-7.
• [2]Brinkel J, Khan MMH, Kraemer A: A systematic review of arsenic exposure and its social and mental health effects with special reference to Bangladesh. Int J Environ Res Public Health 2009, 6:1609-19.
• [3]Das AK, Dewanjee S, Sahu R, Dua TK, Gangopadhyay M, Sinha MK: Protective effect of Corchorus olitorius leaves against arsenic-induced oxidative stress in rat brain. Environ Toxicol Pharmacol 2010, 29:64-9.
• [4]Ratnaike RN: Acute and chronic arsenic toxicity. Postgrad Med J 2003, 79:391-6.
• [5]Rizwan S, Naqshbandi A, Farooqui Z, Khan AA, Khan F: Protective effect of dietary flaxseed oil on arsenic-induced nephrotoxicity and oxidative damage in rat kidney. Food Chem Toxicol 2014, 68:99-107.
• [6]Dutta M, Ghosh D, Ghosh AK, Bose G, Chattopadhyay A, Rudra S, et al.: High fat diet aggravates arsenic induced oxidative stress in rat heart and liver. Food Chem Toxicol 2014, 66:262-77.
• [7]Mehta A, Flora SJS: Possible role of metal redistribution, hepatotoxicity and oxidative stress in chelating agents induced hepatic and renal metallothionein in rats. Food Chem Toxicol 2001, 39:1039-43.
• [8]Aposhian HV, Aposhian MM: Meso-2, 3-dimercapto-succinic acid: chemical, pharmacological and toxicological properties of an orally effective metal chelating agent. Ann Rev Pharmacol Toxicol 1990, 30:279-306.
• [9]Howard G: Arsenic, drinking-water and health risk substitution in arsenic mitigation: a discussion paper. World Health Organization, Geneva; 2003.
• [10]Malalavidhane TS, Wickramasinghe SMDN, Jansz ER: Oral hypoglycaemic activity of Ipomoea aquatica. J Ethnopharmacol 2000, 72:293-8.
• [11]Badruzzaman SM, Husain W: Some aquatic and marshy land medicinal plants from Hardoi district of Uttar Pradesh. Fitoterapia 1992, 63:245-7.
• [12]Samuelsson G, Farah MH, Claeson P, Hagos M, Thulin M, Hedberg O, et al.: Inventory of plants used in traditional medicine in Somalia: II. Plants of the Families Combretaceae to Labiatae. J Ethnopharmacol 1992, 37:47-70.
• [13]Chopra RN, Nayar SL, Chopra IC: Glossary of Indian medicinal plants. Council of Scientific & Industrial Research, New Delhi, India; 1956.
• [14]Vasu K, Goud JV, Suryam A, Charya MAS: Biomolecular and phytochemical analyses of three aquatic angiosperms. Afr J Microbiol Res 2009, 3:418-21.
• [15]Meda A, Lamien CE, Romito M, Millogo J, Nacoulma OJ: Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chem 2005, 91:571-7.
• [16]McDonald S, Prenzler PD, Autolovich M, Robards K: Phenolic content and anti-oxidant activity of olive extract. Food Chem 2001, 73:73-84.
• [17]Obadoni BO, Ochuko PO: Phytochemical studies and comparative efficacy of crude extracts of some homeostatic plants in Edo and Delta States of Nigeria. Global J Pure Appl Sci 2002, 8:203-8.
• [18]Yemm EW, Willis AJ: The estimation of carbohydrates in plant extracts by anthrone. Biochem J 1954, 57:508-14.
• [19]Public Health Service (PHS): Public health service policy on humane care and use of laboratory animals. US Department of Health and Human Services, Washington, DC; 1986.
• [20]Sarkar K, Sil PC: A 43 kDa protein from the herb Cajanus indicus L. protects thioacetamide induced cytotoxicity in hepatocytes. Toxicol In Vitro 2006, 20:634-40.
• [21]Pal S, Pal PB, Das J, Sil PC: Involvement of both intrinsic and extrinsic pathways in hepatoprotection of arjunolic acid against cadmium induced acute damage in vitro. Toxicol 2011, 283:129-39.
• [22]Mansoor TA, Borralho PM, Dewanjee S, Mulhovo S, Rodrigues CPM, Ferreira MJU: Monoterpene bisindole alkaloids, from the African medicinal plant Tabernaemontana elegans, induce apoptosis in HCT116 human colon carcinoma cells. J Ethnopharmacol 2013, 149:463-70.
• [23]LeBel CP, Bondy SC: Sensitive and rapid quantitation of oxygen reactive species formation in rat synaptosomes. Neurochem Int 1990, 17:435-40.
• [24]Ohkawa H, Ohishi N, Yagi K: Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979, 95:351-8.
• [25]Uchida K, Stadtman ER: Covalent attachment of 4-hydroxynonenal to glyceraldehydes-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. J Biol Chem 1993, 268:6388-93.
• [26]Ghosh J, Das J, Manna P, Sil PC: Protective effect of the fruits of Terminalia arjuna against cadmium-induced oxidant stress and hepatic cell injury via MAPK activation and mitochondria dependent pathway. Food Chem 2010, 123:1062-75.
• [27]Hissin PJ, Hilf R: A fluorometric method for the determination of oxidized and reduced glutathione in tissues. Anal Biochem 1973, 74:214-6.
• [28]Das AK, Bag S, Sahu R, Dua TK, Sinha MK, Gangopadhyay M, et al.: Protective effect of Corchorus olitorius leaves on sodium arsenite-induced toxicity in experimental rats. Food Chem Toxicol 2010, 48:326-35.
• [29]Krynitsky AJ: Preparation of biological tissue for determination of arsenic and selenium by graphite furnace atomic absorption spectrometry. Anal Chem 1987, 59:1884-6.
• [30]Zhang Y, Aberg F, Appelkvist EL, Dallner G, Ernster L: Uptake of dietary coenzyme Q supplement is limited in rats. J Nutr 1995, 125:446-53.
• [31]Dewanjee S, Gangopadhyay M, Sahu R, Karmakar R: Cadmium induced pathophysiology: prophylactic role of edible jute (Corchorus olitorius) leaves with special emphasis on oxidative stress and mitochondrial involvement. Food Chem Toxicol 2013, 60:188-98.
• [32]Bera AK, Rana T, Bhattacharya D, Das D, Pan D, Das SK: Sodium arsenite-induced alteration in hepatocytes functions of rat with special emphasis on superoxide dismutase expression pathway and its prevention by mushroom lectin. Basic Clin Pharmacol Toxicol 2011, 109:240-4.
• [33]Kavitha C, Malarvizhi A, Senthil Kumaran S, Ramesh M: Toxicological effects of arsenate exposure on hematological, biochemical and liver transaminases activity in an Indian major carp, Catla catla. Food Chem Toxicol 2010, 48:2848-54.
• [34]Mohanta RK, Garg AK, Dass RS: Effect of vitamin E supplementation on arsenic induced alteration in blood biochemical profile, oxidant/antioxidant status, serum cortisol level and retention of arsenic and selenium in goats. J Trace Elem Med Biol 2015, 29:188-94.
• [35]Watanabe T, Hirano S: Metabolism of arsenic and its toxicological relevance. Arch Toxicol 2013, 87:969-79.
• [36]Dewanjee S, Das AK, Sahu R, Gangopadhyay M: Antidiabetic activity of Diospyros peregrina fruit: Effect on hyperglycemia, hyperlipidemia and augmented oxidative stress in experimental type 2 diabetes. Food Chem Toxicol 2009, 47:2679-85.
• [37]Dewanjee S, Sahu R, Karmakar S, Gangopadhyay M: Toxic effects of lead exposure in Wistar rats: Involvement of oxidative stress and the beneficial role of edible jute (Corchorus olitorius) leaves. Food Chem Toxicol 2013, 55:78-91.
• [38]Kishi T, Takahashi T, Usui A, Okamoto T: Ubiquinone redox cycle as a cellular antioxidant defense system. Biofactors 1999, 10:131-8.
• [39]Dewanjee S, Gangopadhyay M, Das U, Sahu R, Samanta A, Banerjee P: Signal transducer and oxidative stress mediated modulation of phenylpropanoid pathway to enhance rosmarinic acid biosynthesis in fungi elicited whole plant culture of Solenostemon scutellarioides. Enzyme Microb Technol 2014, 66:1-9.
• [40]Zhang W, Xue J, Ge M, Yu M, Liu L, Zhang Z: Resveratrol attenuates hepatotoxicity of rats exposed to arsenic trioxide. Food Chem Toxicol 2013, 51:87-92.
• [41]Moradkhani S, Ayatollahi AM, Ghanadian M, Moin MR, Razavizadeh M, Shahlaei M: Phytochemical analysis and metal-chelation activity of Achillea tenuifolia Lam. Iran J Pharm Res 2012, 11:177-83.
• [42]Xia HL, Chi XY, Yan ZJ, Cheng WW: Enhancing plant uptake of polychlorinated biphenyls and cadmium using tea saponin. Bioresour Technol 2009, 100:4649-53.
• [43]Cooke MS, Evans MD, Dizdaroglu M, Lunec J: Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 2003, 17:1195-214.
• [44]Forbes-Hernandez TY, Giampieri F, Gasparrini M, Mazzoni L, Quiles JL, Alvarez-Suarez JM, et al.: The effects of bioactive compounds from plant foods on mitochondrial function: A focus on apoptotic mechanisms. Food Chem Toxicol 2014, 68:154-82.
• [45]Hill MM, Adrain C, Duriez PJ, Creagh EM, Martin SJ: Analysis of the composition, assembly kinetics and activity of native Apaf-1 apoptosomes. EMBO J 2002, 23:2134-45.
• [46]Khanra R, Dewanjee S, Dua TK, Sahu R, Gangopadhyay M, De Feo V, et al.: (Malvaceae) leaf extract attenuates diabetes induced nephropathy and cardiomyopathy via inhibition of oxidative stress and inflammatory response. J Transl Med 2015, 13:6. BioMed Central Full Text
• [47]Choi YJ, Kang JS, Park JH, Lee YJ, Choi JS, Kang YH: Polyphenolic flavonoids differ in their antiapoptotic efficacy in hydrogen peroxide-treated human vascular endothelial cells. J Nutr 2003, 133:985-91.
• [48]Khanduja KL, Avti PK, Kumar S, Mittal N, Sohi KK, Pathak CM: Anti-apoptotic activity of caffeic acid, ellagic acid and ferulic acid in normal human peripheral blood mononuclear cells: a Bcl-2 independent mechanism. Biochim Biophys Acta 2006, 1760:283-9.
• [49]Sohi KK, Mittal N, Hundal MK, Khanduja KL: Gallic acid, an antioxidant, exhibits antiapoptotic potential in normal human lymphocytes: A Bcl-2 independent mechanism. J Nutr Sci Vitaminol 2003, 49:221-7.
• [50]Singh S, Rana SV: Amelioration of arsenic toxicity by L-Ascorbic acid in laboratory rat. J Environ Biol 2007, 28:377-84.
• [51]Owumi SE, Odunola OA, Gbadegesin MA, Nulah KL: Protective effect of Juglans nigra on sodium arsenite-induced toxicity in rats. Pharmacognosy Res 2013, 5:183-8.