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Anti-Cancer Agents in Medicinal Chemistry


ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Research Article

Protection against Mitochondrial Oxidative-Stress by Flesh-Extract of Edible Freshwater Snail Bellamya bengalensis Prevents Arsenic Induced DNA and Tissue Damage

Author(s): Sk. Sajed Ali, Nandita Medda, Sangita M. Dutta, Ritesh Patra and Smarajit Maiti*

Volume 20 , Issue 10 , 2020

Page: [1266 - 1273] Pages: 8

DOI: 10.2174/1871520620666200410081535

Price: $65


Aims: Arsenic has carcinogenic properties because of the formation of Reactive Oxygen Species (ROS). ROS damages different macromolecules, tissues and organs, and severely exhausts cellular antioxidants.

Background: Cytosolic and mitochondrial contribution of ROS production by arsenic are not well reported. In regard to the issues of therapy against arsenic or any other toxicity, natural product has gained its popularity due to its less side-effects and non-invasive nature.

Objectives: Here, as an ethnomedicine, the flesh-extract (BBE; 100mg/100g bw) of Bellamya bengalensis (an aquatic mollusk) was applied in arsenic intoxicated (0.6 ppm/100g bw/for 28 days alone or in combination with BBE) experimental rats. Our objective was to study the anti-oxidative and anti-apoptotic role of BBE in hepato-gastrointestinal tissue damage by arsenic.

Methods: DNA fragmentation assay, catalase activity (gel-zymogram assay) suggests that BBE has a strong protective role against arsenic toxicity, which is decisively demonstrated in hepatic histoarchitecture study by HE (hematoxylin and eosin) staining and by intestinal PAS (Periodic Acid Schiff) staining.

Results: Measurement of mitochondrial-membrane-potential by fluorescent microcopy clearly demonstrated less membrane damage and lower release of the redox-active inner-membrane product (cytochrome-C, ubiquinone, etc.) in BBE supplemented group compared to that of the only arsenic fed group. The present study clearly suggests that mitochondrial disintegrity is one of the major causes of ROS mediated tissue damage by arsenic.

Conclusion: This study also offers an option for prevention/treatment against arsenic toxicity and its carcinogenicity by widely available low-cost, non-invasive Bellamya extract by protecting cytoskeleton, DNA and mitochondria in the cell.

Keywords: Arsenic toxicity, mitochondrial oxidative damage, carcinogenesis, DNA damages, oxidative stress and apoptosis, chemotherapeutics by Bellamya bengalensis.

Graphical Abstract
Ratnaike, R.N. Acute and chronic arsenic toxicity. Postgrad. Med. J., 2003, 79(933), 391-396.
[] [PMID: 12897217]
Németi, B.; Gregus, Z. Reduction of arsenate to arsenite in hepatic cytosol. Toxicol. Sci., 2002, 70(1), 4-12.
[] [PMID: 12388829]
Lawley, S.D.; Yun, J.; Gamble, M.V.; Hall, M.N.; Reed, M.C.; Nijhout, H.F. Mathematical modeling of the effects of glutathione on arsenic methylation. Theor. Biol. Med. Model, 2014, 11, 20.
Mazumder, D.N. Effect of chronic intake of arsenic-contaminated water on liver. Toxicol. Appl. Pharmacol., 2005, 206(2), 169-175.
[] [PMID: 15967205]
Maiti, S.; Chatterjee, A.K. Differential response of cellular antioxidant mechanism of liver and kidney to arsenic exposure and its relation to dietary protein deficiency. Environ. Toxicol. Pharmacol., 2000, 8(4), 227-235.
[] [PMID: 10996542]
Tseng, C.H.; Tseng, C.P.; Chiou, H.Y.; Hsueh, Y.M.; Chong, C.K.; Chen, C.J. Epidemiologic evidence of diabetogenic effect of arsenic. Toxicol. Lett., 2002, 133(1), 69-76.
[] [PMID: 12076511]
Gomes, A.; Alam, M.A.; Datta, P.; Bhattacharya, S.; Gomes, A. Hepatoprotective activity of the edible snail (Bellamia bengalensis) flesh extract in carbon tetrachloride induced hepatotoxicity in rats. J. Ethnopharmacol., 2011, 138(1), 228-232.
[] [PMID: 21945824]
Maiti, S.; Chattopadhyay, S.; Acharyya, N.; Deb, B. Emblica officinalis (amla) ameliorates arsenic-induced liver damage via DNA protection by antioxidant systems. Mol. Cell. Toxicol., 2014, 10, 75.
Kun, E.; Kirsten, E.; Piper, W.N. Stabilization of mitochondrial functions with digitonin. Methods Enzymol., 1979, 55, 115-118.
[] [PMID: 459838]
Baracca, A.; Sgarbi, G.; Solaini, G.; Lenaz, G. Rhodamine 123 as a probe of mitochondrial membrane potential: Evaluation of proton flux through F(0) during ATP synthesis. Biochim. Biophys. Acta, 2003, 1606(1-3), 137-146.
[] [PMID: 14507434]
Weydert, C.J.; Cullen, J.J. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat. Protoc., 2010, 5(1), 51-66.
[] [PMID: 20057381]
Garcia-Martinez, V.; Macias, D.; Gañan, Y.; Garcia-Lobo, J.M.; Francia, M.V.; Fernandez-Teran, M.A.; Hurle, J.M. Internucleosomal DNA fragmentation and programmed cell death (apoptosis) in the interdigital tissue of the embryonic chick leg bud. J. Cell Sci., 1993, 106(Pt 1), 201-208.
[PMID: 8270624]
Kim, S.K.; Pallela, R. Medicinal foods from marine animals: current status and prospects. Adv. Food Nutr. Res., 2012, 65, 1-9.
[] [PMID: 22361177]
Shabelnikov, S.; Kiselev, A. Cysteine-rich atrial secretory protein from the snail Achatina achatina: Purification and structural characterization. PLoS One, 2015, 10(10), e0138787.
[] [PMID: 26444993]
Besra, S.E.; Ray, M.M.; Dey, S.; Roy, S.; Deb, N. Apoptogenic activity of secretion extract of Bellamya bengalensis f. annandalei via mitochondrial mediated caspase cascade on human leukemic cell lines. Int. J. Pharm. Sci. Rev. Res., 2013, 20, 146-152.
Mitchell, R.A.; Chang, B.F.; Huang, C.H.; DeMaster, E.G. Inhibition of mitochondrial energy-linked functions by arsenate. Evidence for a nonhydrolytic mode of inhibitor action. Biochemistry, 1971, 10(11), 2049-2054.
[] [PMID: 4327397]
Gresser, M.J. ADP-arsenate. Formation by submitochondrial particles under phosphorylating conditions. J. Biol. Chem., 1981, 256(12), 5981-5983.
[PMID: 7240187]
Chakraborti, D.; Mukherjee, M.; Maity, J. Ethno-medicinal importance of viviparous gastropod, Bellamya bengalensis (Lamarck, 1822) in terms of estimation of its proximate protein and amino acid composition. Int. J. Sci. Res. (Ahmedabad), 2015, 4, 178-180.
Maiti, S. Arsenic-induced mutagenesis and carcinogenesis: A possible mechanism. In: Hand book of Arsenic Toxicology; Academic Press, 2015, pp. 233-265.
Halliwell, B.; Chirico, S. Lipid peroxidation: its mechanism, measurement, and significance. Am. J. Clin. Nutr., 1993, 57(5)(Suppl.), 715S-724S.
[] [PMID: 8475889]
Sharma, A.; Sharma, M.K.; Kumar, M. Modulatory role of Emblica officinalis fruit extract against arsenic induced oxidative stress in Swiss albino mice. Chem. Biol. Interact., 2009, 180(1), 20-30.
[] [PMID: 19428342]
Ali, S.S.; Acharyya, N.; Maiti, S. Promising anti-oxidative therapeutic potentials of edible freshwater snail Bellamya bengalensis extract against arsenic-induced rat hepatic tissue and DNA damage. Int. J. Aquat. Biol., 2016, 4(4), 239.
Stachowicz, M.; Hiemstra, T.; van Riemsdijk, W.H. Multi competitive interaction of As(III) and As(V) oxyanions with Ca(2+), Mg(2+), PO(3-)(4), and CO(2-)(3) ions on goethite. J. Colloid Interface Sci., 2008, 320(2), 400-414.
[] [PMID: 18272166]
Delnomdedieu, M.; Basti, M.M.; Otvos, J.D.; Thomas, D.J. Transfer of arsenite from glutathione to dithiols: A model of interaction. Chem. Res. Toxicol., 1993, 6(5), 598-602.
[] [PMID: 8292735]
Gauri, S.S.; Mandal, S.M.; Pati, B.R.; Dey, S. Purification and structural characterization of a novel antibacterial peptide from Bellamya bengalensis: activity against ampicillin and chloramphenicol resistant Staphylococcus epidermidis. Peptides, 2011, 32(4), 691-696.
[] [PMID: 21262297]
Karuppusamy, S.; Muthuraja, G. Radical scavenging activities of Heracleum aquilegifolium Wight (Apiaceae) fruit oils in vitro. Z. Natforsch. C J. Biosci., 2010, 65(11-12), 653-659.
[] [PMID: 21319706]
Niki, E. Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence. Free Radic. Biol. Med., 2014, 66, 3-12.
[] [PMID: 23557727]
Chitrapriya, N.; Park, J.; Wang, W.; Lee, H.; Kim, S.K. Photo-induced DNA scission by Cu(ii)-meso-tetrakis(n-N-methylpyridiniumyl)porphyrins (n = 2, 3, 4) and their binding modes to supercoiled DNA. Metallomics, 2012, 4(5), 417-421.
[] [PMID: 22522944]
Acharyya, N.; Chattopadhyay, S.; Maiti, S. Chemoprevention against arsenic-induced mutagenic DNA breakage and apoptotic liver damage in rat via antioxidant and SOD1 upregulation by green tea (Camellia sinensis) which recovers broken DNA resulted from arsenic-H2O2 related in vitro oxidant stress. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev., 2014, 32(4), 338-361.
Bhattacharya, S.; Chakraborty, M.; Bose, M.; Mukherjee, D.; Roychoudhury, A.; Dhar, P.; Mishra, R. Indian freshwater edible snail Bellamya bengalensis lipid extract prevents T cell mediated hypersensitivity and inhibits LPS induced macrophage activation. J. Ethnopharmacol., 2014, 157, 320-329.
[] [PMID: 25291010]
Muriel, P.; Deheza, R. Fibrosis and glycogen stores depletion induced by prolonged biliary obstruction in the rat are ameliorated by metadoxine. Liver Int., 2003, 23(4), 262-268.
[] [PMID: 12895266]
Rodríguez-González, H.; Hernández-Llamas, A.; Villarreal, H.; Saucedo, P.E.; García-Ulloa, M.; Rodríguez-Jaramillo, C. Gonadal development and biochemical composition of female crayfish Cherax quadricarinatus (Decapoda: Parastacidae) in relation to the Gonadosomatic Index at first maturation. Aquaculture, 2006, 254, 637-645.
Lowry, O.H.; Rosebrough, N.J.; Farr, A.L.; Randall, R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951, 193(1), 265-275.
[PMID: 14907713]
Bergström, J.; Fürst, P.; Norée, L.O.; Vinnars, E. Intracellular free amino acid concentration in human muscle tissue. J. Appl. Physiol., 1974, 36(6), 693-697.
[] [PMID: 4829908]
Motomizu, S.; Wakimoto, T.; Tôei, K. Solvent extraction spectrophotometric determination of phosphate with molybdate and malachite green in river water and sea-water. Talanta, 1984, 31(4), 235-240.
[] [PMID: 18963579]
Barrows, J.N.; Jameson, G.B.; Pope, M.T. Structure of a heteropoly blue. The four-electron reduced. beta.-12-molybdophosphate anion. J. Am. Chem. Soc., 1985, 107, 1771-1773.
Hazari, M.A.H.; Arifuddin, M.S.; Muzzakar, S.; Reddy, V.D. Serum calcium level in hypertension. N. Am. J. Med. Sci., 2012, 4(11), 569-572.
[] [PMID: 23181228]
Forman, H.J. Critical methods in Free radical biology and medicine. Free Radic. Biol. Med., 2009, 47(Suppl. 2), S207.
[] [PMID: 19765645]

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