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Protective Role of Moringa oleifera (Sajina) Seed on Arsenic-Induced Hepatocellular Degeneration in Female Albino Rats

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Abstract

In an attempt to develop new herbal therapy, an aqueous extract of the seed of Moringa oleifera was used to screen the effect on arsenic-induced hepatic toxicity in female rat of Wistar strain. Subchronic exposure to sodium arsenite (0.4 ppm/100 g body weight/day via drinking water for a period of 24 days) significantly increased activities of hepatic and lipid function markers such as alanine transaminase, aspartate transaminase, cholesterol, triglycerides, LDL along with a decrease in total protein and HDL. A notable distortion of hepatocellular histoarchitecture was prominent with a concomitant increase in DNA fragmentation following arsenic exposure. A marked elevation of lipid peroxidation in hepatic tissue was also evident from the hepatic accumulation of malondialdehyde and conjugated dienes along with suppressed activities in the antioxidant enzymes such as superoxide dismutase and catalase. However, co-administration of aqueous seed extract of M. oleifera (500 mg/100 g body weight/day for a period of 24 days) was found to significantly prevent the arsenic-induced alteration of hepatic function markers and lipid profile. Moreover, the degeneration of histoarchitecture of liver found in arsenic-treated rats was protected along with partial but definite prevention against DNA fragmentation induction. Similarly, generation of reactive oxygen species and free radicals were found to be significantly less along with restored activities of antioxidant enzymes in M. oleifera co-administered group with comparison to arsenic alone treatment group. The present investigation offers strong evidence for the hepato-protective and antioxidative efficiencies of M. oleifera seed extract against oxidative stress induced by arsenic.

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References

  1. Hartwig A, Groblinghoff UD, Beyersmann D, Natarajan AT, Filon R, Mullenders LH (1997) Interaction of arsenic (III) with nucleotide excision repair in UV-irradiated human fibroblasts. Carcinogenesis 18:399–405

    Article  PubMed  CAS  Google Scholar 

  2. Bode AM, Dong Z (2002) The paradox of arsenic: molecular mechanisms of cell transformation and chemotherapeutic effects. Crit Rev Oncol Hematol 42:5–24

    Article  PubMed  Google Scholar 

  3. Yih L, Peck K, Lee T (2002) Changes in gene expression profiles of human fibroblasts in response to sodium arsenite treatment. Carcinogenesis 23:867–876

    Article  PubMed  CAS  Google Scholar 

  4. Chowdhury TR, Mandal BK, Samanta G, Basv GK, Chowdhury PP, Chanda CR, Karan NK, Lodh D, Dhar RK, Das D (1997) Arsenic in ground water in six districts of West Bengal, India—the biggest arsenic calamity in the world, the status report up to August 1995. In: Abernathy CO, Calderson RL, Chappell WR (eds) Arsenic exposure and health effects. Chapman and Hall, New York, pp 93–111

    Google Scholar 

  5. Mukherjee SC, Saha KC, Pati S, Dutta RN, Rahman MM, Sengupta MK, Ahamed S, Lodh D, Das B, Hossain MA, Nayak B, Mukherjee A, Chakraborti D, Dutta SK, Palit SK, Kaies I, Barua AK, Asad KA (2005) Murshidabad—one of the nine groundwater arsenic-affected districts of West Bengal, India. Part II: dermatological, neurological, and obstetric findings. Clin Toxicol Phila 43:835–848

    Article  PubMed  CAS  Google Scholar 

  6. Klaassen CD (1990) Heavy metals and heavy metal antagonists. In: Goodman GA, Rall TW, Nies AS, Taylor P (eds) The pharmaceutical basis of therapeutics. Pergamen Press, New York, pp 1602–1605

    Google Scholar 

  7. Longnecker MP, Daniels JL (2001) Environmental contaminants as etiologic factors for diabetes. Environ Health Perspect 109 6(Suppl.):871–876

    Article  Google Scholar 

  8. Tseng CH, Tseng CP, Chiou HY, Hsueh YM, Chong CK, Chen CJ (2002) Epidemiologic evidence of diabetogenic effect of arsenic. Toxicol Lett 133:69–76

    Article  PubMed  CAS  Google Scholar 

  9. Wang A, Holladay SD, Wolf DC, Ahmed SA, Robertson JL (2006) Reproductive and developmental toxicity of arsenic in rodents: a review. Int J Toxicol 25:319–331

    Article  PubMed  Google Scholar 

  10. Sarkar M, Chaudhuri GR, Chattopadhyay A, Biswas NM (2003) Effect of sodium arsenite on spermatogenesis, plasma gonadotrophins and testosterone in rats. Asian J Androl 5:27–31

    PubMed  CAS  Google Scholar 

  11. Chattopadhyay S, Ghosh S, Chaki S, Debnath J, Ghosh D (1999) Effect of sodium arsenite on plasma levels of gonadotrophins and ovarian steroidogenesis in mature albino rats: duration dependent response. J Toxicol Sci 24:425–431

    PubMed  CAS  Google Scholar 

  12. Ghosh D, Chattopadhyay S, Debnath J (1999) Effect of sodium arsenite on adrenocortical activity in immature female rats: evidence of dose dependent response. J Environ Sci 11:419–422

    CAS  Google Scholar 

  13. Saha AK (1991) Pollution in ground water in West Bengal. Final report: Steering Committee Arsenic Investigation Project, PHE Dept Government of West Bengal India. pp 1–56.

  14. Malhotra P, Varma N, Arora N, Das R, Nath A, Patel FD, Varma S (2010) Treatment of therapy related acute promyelocytic leukemia with the combination of all trans retinoic acid and arsenic trioxide without chemotherapy: a series of three patients. Leuk Lymphoma 51:933–936

    Article  PubMed  CAS  Google Scholar 

  15. Tabacova S, Hunter ES, Balabaeva L (1992) Potential role of oxidative damage in developmental toxicity of arsenic. In: Abernathy CO, Calderon RL, Chappell WR (eds) Arsenic exposure and health effects. Chapman and Hall, London, pp 135–144

    Google Scholar 

  16. Yamanaka K, Hoshino M, Okamoto M, Sawamura R, Hasegawa A, Okada S (1990) Induction of DNA damage by dimethylarsine, a metabolite of inorganic arsenics, is for the major part likely due to its peroxyl radical. Biochem Biophys Res Commun 168:58–64

    Article  PubMed  CAS  Google Scholar 

  17. Kato K, Hayashi H, Hasegawa A, Yamanaka K, Okada S (1994) DNA damage induced in cultured human alveolar (L-32) cells by exposure to dimethylarsinic acid. Environ Health Perspect 102:285–288

    PubMed  CAS  Google Scholar 

  18. Greenwel P, Dominguez-Rosals JA, Mavi G, Rivas-Estilla AM, Rojkind M (2000) Hydrogen peroxide: a link between acetaldehyde-elicited alpha 1 (I) collagen gene up-regulation and oxidative stress in mouse hepatic stellate cells. Hepatol 31:109–116

    Article  CAS  Google Scholar 

  19. Mandal AK, Das S, Basu MK, Chakrabarti RN, Das N (2007) Hepatoprotective activity of liposomal flavonoid against arsenite-induced liver fibrosis. J Pharmacol Exp Ther 320:994–1001

    Article  PubMed  CAS  Google Scholar 

  20. Chattopadhyay S, Misro M, Ghosh S, Debnath J, Ghosh D (2000) Effect of α-tocopherol succinate (vitamin E) on sodium arsenite induced ovarian steroidogenic function and plasma levels of gonadotrophins in mature albino rats. Toxic Subst Mech 19:137–150

    Article  CAS  Google Scholar 

  21. Chattopadhyay S, Ghosh S, Debnath J, Ghosh D (2001) Protection of sodium arsenite-induced ovarian toxicity by coadministration of L-ascorbate (vitamin C) in mature Wistar strain rat. Arch Environ Contam Toxicol 1:83–89

    Article  Google Scholar 

  22. Chattopadhyay S, Pal Ghosh S, Ghosh D, Debnath J (2003) Effect of dietary co-administration of sodium selenite on sodium arsenite-induced ovarian and uterine disorders in mature albino rats. Toxicol Sci 75:412–422

    Article  PubMed  CAS  Google Scholar 

  23. Manna P, Sinha M, Sil PC (2007) Protection of arsenic-induced hepatic disorder by arjunolic acid. Basic Clin Pharmacol Toxicol 101:333–338

    Article  PubMed  CAS  Google Scholar 

  24. Chattopadhyay S, Ghosh D (2010) The involvement of hypophyseal-gonadal and hypophyseal-adrenal axis in arsenic mediated ovarian and uterine toxicity modulation by hCG. J Biochem Mol Toxicol 24:29–41

    Article  PubMed  CAS  Google Scholar 

  25. Chattopadhyay S, Ghosh D (2010) Role of dietary GSH in the amelioration of sodium arsenite-induced ovarian and uterine disorders. Reprod Toxicol doi:10.1016/jreprotox2010.05.002 (in press)

  26. Inns RH, Rice P, Bright JE, Marrs TC (1990) Evaluation of the efficacy of dimercapto chelating agents for the treatment of systemic organic arsenic poisoning in rabbits. Hum Exp Toxicol 9:215–220

    Article  PubMed  CAS  Google Scholar 

  27. Flora SJ, Bhadauria S, Kannan GM, Singh N (2007) Arsenic induced oxidative stress and the role of antioxidant supplementation during chelation: a reiew. J Environ Biol 28:333–347

    PubMed  CAS  Google Scholar 

  28. Verma R, Trivedi M, Keshwani H, Choksi P, Sangai N (2007) Ameliorative effect of three medicinal plants (P fraternus Terminelia a and Moringa oleifera) on arsenic trioxide induced alteration of lipid peroxidation and protein contents in chicken liver homogenate: an in vitro study. Acta Pol Pharm 64:417–421

    PubMed  CAS  Google Scholar 

  29. Anwar F, Latif S, Ashraf M, Gilani AH (2007) Moringa oleifera: a food plant with multiple medicinal uses. Phytother Res 21:17–25

    Article  PubMed  CAS  Google Scholar 

  30. Ndiaye M, Dieye AM, Mariko F, Tall A, Sall Diallo A, Faye B (2002) Contribution to the study of the anti-inflammatory activity of Moringa oleifera (Moringaceae). Dakar Méd 47:210–212

    PubMed  CAS  Google Scholar 

  31. Ndong M, Uehara M, Katsumata S, Sato S, Suzuki K (2007) Preventive effects of Moringa oleifera (Lam) on hyperlipidemia and hepatocyte ultrastructural changes in iron deficient rats. Biosci Biotechnol Biochem 71:1826–1833

    Article  PubMed  CAS  Google Scholar 

  32. Fakurazi S, Hairuszah I, Nanthini U (2008) Moringa oleifera Lam prevents acetaminophen induced liver injury through restoration of glutathione level. Food Chem Toxicol 46:2611–26155

    Article  PubMed  CAS  Google Scholar 

  33. Hamza AA (2009) Ameliorative effects of Moringa oleifera Lam seed extract on liver fibrosis in rats. Food Chem Toxicol (in press)

  34. Gupta R, Dubey DK, Kannan GM, Flora SJ (2007) Concomitant administration of Moringa oleifera seed powder in the remediation of arsenic-induced oxidative stress in mouse. Cell Biol Int 31:44–56

    Article  PubMed  CAS  Google Scholar 

  35. 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 (in press)

  36. Verma AR, Vijay Kumar M, Mathela CS, Rao CV (2009) In vitro and in vivo antioxidant properties of different fractions of Moringa oleifera leaves. Food Chem Toxicol 47:2196–2201

    Article  PubMed  CAS  Google Scholar 

  37. Bergmeyer HU, Scheibe P, Wahlefeld AW (1978) Optimization of methods for aspartate aminotransferase and alanine aminotransferase. Clin Chem 24:58–73

    PubMed  CAS  Google Scholar 

  38. Macomb RB, Bowers GN Jr (1972) Study of optimum buffer conditions for measuring alkaline phosphatase activity in human serum. Clin Chem 18:97–104

    Google Scholar 

  39. Allain CC, Poon LS, Chan CS, Richmond W, Fu PC (1974) Enzymatic determination of total serum cholesterol. Clin Chem 20:470–475

    PubMed  CAS  Google Scholar 

  40. Warnick GR, Nguyen T, Albers AA (1985) Comparison of improved precipitation methods for quantification of high-density lipoprotein cholesterol. Clin Chem 31:217–222

    PubMed  CAS  Google Scholar 

  41. Werner M, Gabrielson DG, Eastman J (1981) Ultramicro determination of serum triglycerides by bioluminescent assay. Clin Chem 27:268–271

    PubMed  CAS  Google Scholar 

  42. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem 18:499–502

    PubMed  CAS  Google Scholar 

  43. Okhawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  Google Scholar 

  44. Jendryczko A, Drózdz M (1988) Lipid peroxidation in the nuclear fraction of rat lungs induced by hydralazine. Neoplasma 35:37–40

    PubMed  CAS  Google Scholar 

  45. Paoletti F, Mocali A, Aldinucci D (1990) Superoxide-driven NAD(P)H oxidation induced by EDTA-manganese complex and mercaptoethanol. Chem Biol Interact 76:3–18

    Article  PubMed  CAS  Google Scholar 

  46. Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389–394

    Article  PubMed  CAS  Google Scholar 

  47. Wyllie A, Kerr JFR, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68:251–306

    Article  PubMed  CAS  Google Scholar 

  48. Compton MM (1992) A biochemical hallmark of apoptosis: internucleosomal degradation of the genome. Cancer Metastasis Rev 11:105–119

    Article  PubMed  CAS  Google Scholar 

  49. Axelson O, Dahlgren E, Jansson CD, Rehnlund SO (1978) Arsenic exposure and mortality: a case-referent study from a Swedish copper smelter. Br J Ind Med 35:8–15

    PubMed  CAS  Google Scholar 

  50. Liu J, Zheng B, Aposhian HV, Zhou Y, Chen ML, Zhang A, Waalkes MP (2002) Chronic arsenic poisoning from burning high-arsenic-containing coal in Guizhou China. Environ Health Perspect 110:119–122

    Article  PubMed  Google Scholar 

  51. McVicker BL, Tuma PL, Kharbanda KK, Lee SM, Tuma DJ (2009) Relationship between oxidative stress and hepatic glutathione levels in ethanol-mediated apoptosis of polarized hepatic cells. World J Gastroenterol 15:2609–2616

    Article  PubMed  CAS  Google Scholar 

  52. Palaniappan P, Vijayasundaram V (2008) FTIR study of arsenic induced biochemical changes on the liver tissues of fresh water fingerlings Labeo rohita. Rom J Biophys 18:135–144

    CAS  Google Scholar 

  53. Li GX, Pei QL, Gao Y, Liu KM, Nie JS, Han G, Qiu YL, Zhang WP (2007) Protective effects of hepatocellular canalicular conjugate export pump (Mrp2) on sodium arsenite-induced hepatic dysfunction in rats. Exp Toxicol Pathol 58:447–453

    Article  PubMed  CAS  Google Scholar 

  54. Zaldívar R, Prunés L, Ghai GL (1981) Arsenic dose in patients with cutaneous carcinomata and hepatic haemangio-endothelioma after environmental and occupational exposure. Arch Toxicol 47:145–154

    Article  PubMed  Google Scholar 

  55. Yousef MI, El-Demerdash FM, Radwan FM (2008) Sodium arsenite induced biochemical perturbations in rats: ameliorating effect of curcumin. Food Chem Toxicol 46:3506–3511

    Article  PubMed  CAS  Google Scholar 

  56. Sinha D, Roy S, Roy M (2010) Antioxidant potential of tea reduces arsenite induced oxidative stress in Swiss albino mice. Food Chem Toxicol 48:1032–1039

    Article  PubMed  CAS  Google Scholar 

  57. Avani G, Rao MV (2007) Genotoxic effects in human lymphocytes exposed to arsenic and vitamin A. Toxicol In Vitro 21:626–631

    Article  PubMed  CAS  Google Scholar 

  58. Kibriya MG, Jasmine F, Argos M, Verret WJ, Rakibuz-Zaman M, Ahmed A, Parvez F, Ahsan H (2007) Changes in gene expression profiles in response to selenium supplementation among individuals with arsenic-induced pre-malignant skin lesions. Toxicol Lett 169:162–176

    Article  PubMed  CAS  Google Scholar 

  59. Argos M, Kibriya MG, Parvez F, Jasmine F, Rakibuz-Zaman M, Ahsan H (2006) Gene expression profiles in peripheral lymphocytes by arsenic exposure and skin lesion status in a Bangladeshi population. Cancer Epidemiol Biomark Prev 15:1367–1375

    Article  CAS  Google Scholar 

  60. Xue W, Wang Z, Chen Q, Chen J, Yang H, Xue S (2010) High selenium status in individuals exposed to arsenic through coal-burning in Shaanxi (PR of China) modulates antioxidant enzymes heme oxygenase-1 and DNA damage. Clin Chim Acta (in press)

  61. Roy M, Sinha D, Mukherjee S, Paul S, Bhattacharya RK (2008) Protective effect of dietary phytochemicals against arsenite induced genotoxicity in mammalian V79 cells. Indian J Exp Biol 46:690–697

    PubMed  CAS  Google Scholar 

  62. Maiti S, Chatterjee AK (2001) Effects on levels of glutathione and some related enzymes in tissues after an acute arsenic exposure in rats and their relationship to dietary protein deficiency. Arch Toxicol 75:531–537

    Article  PubMed  CAS  Google Scholar 

  63. Li M, Cai JF, Chiu JF (2002) Arsenic induces oxidative stress and activates stress gene expressions in cultured lung epithelial cells. J Cell Biochem 87:29–38

    Article  PubMed  CAS  Google Scholar 

  64. Shila S, Subathra M, Devi MA, Panneerselvam C (2005) Arsenic intoxication-induced reduction of glutathione level and of the activity of related enzymes in rat brain regions reversal by dl-alpha-lipoic acid. Arch Toxicol 79:140–146

    Article  PubMed  CAS  Google Scholar 

  65. Santra A, Chowdhury A, Ghataka S, Biswas A, Dhalia GK (2007) Arsenic induces apoptosis in mouse liver is mitochondria dependent and is abrogated by N-acetylcysteine. Toxicol Appl Pharmacol 220:146–155

    Article  PubMed  CAS  Google Scholar 

  66. Atawodi SE, Atawodi JC, Idakwo GA, Pfundstein B, Haubner R, Wurtele G, Bartsch H, Owen RW (2010) Evaluation of the polyphenol content and antioxidant properties of methanol extracts of the leaves, stem, and root barks of Moringa oleifera Lam. J Med Food 13:710–716

    Article  PubMed  CAS  Google Scholar 

  67. Barminas JT, Charles M, Emmanuel D (1998) Mineral composition of non-conventional leafy vegetables. Plant Foods Hum Nutr 53:29–36

    Article  PubMed  CAS  Google Scholar 

  68. Huang GQ, Xiao ZJ (2007) HG-AFS determination of selenium in Moringa oleifera. Guang Pu Xue Yu Guang Pu Fen Xi 27:383–385

    PubMed  Google Scholar 

  69. Freiberger CE, Vanderjagt DJ, Pastuszyn A, Glew RS, Mounkaila G, Millson M, Glew RH (1998) Nutrient content of the edible leaves of seven wild plants from Niger. Plant Foods Hum Nutr 53:57–69

    Article  PubMed  CAS  Google Scholar 

  70. Faizi S, Siddiqui BS, Saleem R, Siddiqui S, Aftab K, Gilani AH (1994) Isolation and structure elucidation of new nitrile and mustard oil glycosides from Moringa oleifera and their effect on blood pressure. J Nat Prod 57:1256–1261

    Article  PubMed  CAS  Google Scholar 

  71. Cheenpracha S, Park EJ, Yoshida WY, Barit C, Wall M, Pezzuto JM, Chang LC (2010) Potential anti-inflammatory phenolic glycosides from the medicinal plant Moringa oleifera fruits. Bioorg Med Chem. doi:10.1016/j.bmc.2010.03.057

    PubMed  Google Scholar 

  72. Doudican NA, Bowling B, Orlow SJ (2010) Enhancement of arsenic trioxide cytotoxicity by dietary isothiocyanates in human leukemic cells via a reactive oxygen species-dependent mechanism. Leuk Res 34:229–234

    Article  PubMed  CAS  Google Scholar 

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Chattopadhyay, S., Maiti, S., Maji, G. et al. Protective Role of Moringa oleifera (Sajina) Seed on Arsenic-Induced Hepatocellular Degeneration in Female Albino Rats. Biol Trace Elem Res 142, 200–212 (2011). https://doi.org/10.1007/s12011-010-8761-7

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