Login Register Cart 0
Generic placeholder image

Drug Metabolism and Bioanalysis Letters

Editor-in-Chief

ISSN (Print): 2949-6810
ISSN (Online): 2949-6829

Back
Journal Home About Journal Editorial Board Current Issue Volumes/Issues
Subscribe
Research Article

Berberine Recovered Oxidative Stress Induced by Sodium Nitrite in Rat Erythrocytes

Author(s): Morteza Akhzari, Mahdi Barazesh*, Sajad Jalili* and Mohammad Mahdi Farzinezhadi Zadeh

Volume 15, Issue 3, 2022

Published on: 18 October, 2022

Page: [192 - 201] Pages: 10

DOI: 10.2174/2949681015666220902114519

Price: $65

Abstract

Objective: Berberine, a plant derived alkaloid, present in Berberis species is well known as one of the most important antioxidants. The current research aimed to study the heamatoprotective characteristics of berberine and clarify its plausible mechanisms against sodium nitrite.

Methods: Forty numbers of male Sprague Dawley rats were categorized into five equal groups, including group 1: control (normal saline); group 2: berberine (100 mg/kg); group 3: sodium nitrite (80 mg/kg); group 4: sodium nitrite (80 mg/kg) plus berberine (50 mg/kg) and group 5: sodium nitrite (80 mg/kg) plus berberine (100 mg/kg) groups. All animals were orally administrated for two months once daily. At the end of the 60th day, blood samples were withdrawn by cardiac puncture and collected in test vials when the animals had been anesthetized with ketamine (70 mg/kg). Then, hemolysate was prepared and the oxidative stress biomarkers, lipid peroxidation, and antioxidant capacity of erythrocytes were evaluated.

Results: Feeding of rats with sodium nitrite remarkably enhanced malondialdehyde (MDA) (p=0.001) levels and considerably reduced the levels of glutathione (GSH) (p=0.001), and also reduced the enzymatic activities of glutathione peroxidase (GPx) (p=0.02), superoxide dismutase (SOD) (p=0.001), glutathione reductase (GR) (p=0.02), and catalase (CAT) (p=0.01). However, the co-administration of these animals with 100 mg/kg of berberine remarkably reverted the values to reach nearly a normal level. While 50 mg/kg berberine failed to restore significantly all of these antioxidant biomarkers at a normal level.

Conclusion: Our results clearly demonstrated that berberine in a dose-dependent manner led to protection against sodium nitrite-induced oxidative injury in rat erythrocytes, which possibly reflects the antioxidant ability of this alkaloid.

Keywords: Berberine, sodium nitrite, oxidative stress, erythrocytes, rat, antioxidant.

« Previous Next »
Graphical Abstract

[1]
Pham-Huy, L.A.; He, H.; Pham-Huy, C. Free radicals, antioxidants in disease and health. Int. J. Biomed. Sci., 2008, 4(2), 89-96.
[PMID: 23675073]
[2]
Pandey, K.B.; Rizvi, S.I. Markers of oxidative stress in erythrocytes and plasma during aging in humans. Oxid. Med. Cell. Longev., 2010, 3(1), 2-12.
[http://dx.doi.org/10.4161/oxim.3.1.10476] [PMID: 20716923]
[3]
Johnson, R.; Goyette, G., Jr; Ravindranath, Y.; Ho, Y. Hemoglobin autoxidation and regulation of endogenous H2O2 levels in erythrocytes. Free Radic. Biol. Med., 2005, 39(11), 1407-1417.
[http://dx.doi.org/10.1016/j.freeradbiomed.2005.07.002] [PMID: 16274876]
[4]
Tsantes, A.E.; Bonovas, S.; Travlou, A.; Sitaras, N.M. Redox imbalance, macrocytosis, and RBC homeostasis. Antioxid. Redox Signal., 2006, 8(7-8), 1205-1216.
[http://dx.doi.org/10.1089/ars.2006.8.1205] [PMID: 16910768]
[5]
Sindelar, J.J.; Milkowski, A.L. Human safety controversies surrounding nitrate and nitrite in the diet. Nitric Oxide, 2012, 26(4), 259-266.
[http://dx.doi.org/10.1016/j.niox.2012.03.011] [PMID: 22487433]
[6]
Milkowski, A.; Garg, H.K.; Coughlin, J.R.; Bryan, N.S. Nutritional epidemiology in the context of nitric oxide biology: A risk–benefit evaluation for dietary nitrite and nitrate. Nitric Oxide, 2010, 22(2), 110-119.
[http://dx.doi.org/10.1016/j.niox.2009.08.004] [PMID: 19748594]
[7]
Bryan, N.S. Nitrite in nitric oxide biology: Cause or consequence? Free Radic. Biol. Med., 2006, 41(5), 691-701.
[http://dx.doi.org/10.1016/j.freeradbiomed.2006.05.019] [PMID: 16895789]
[8]
Butler, A.R.; Feelisch, M. Therapeutic uses of inorganic nitrite and nitrate: From the past to the future. Circulation, 2008, 117(16), 2151-2159.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.107.753814] [PMID: 18427145]
[9]
Jan, A.; Andrew, C.; Jean-Pierre, C.; Eugenia, D.; Alessandro, D.; Maria, L.; Peter, F.; Johanna, F.; Corrado, L.; Philippe, G. Nitrite as undesirable substances in animal feed. EFSA J., 2009, 1017, 1-47.
[10]
Katabami, K.; Hayakawa, M.; Gando, S. Severe methemoglobinemia due to sodium nitrite poisoning. Case Reports Emerg. Med., 2016, 2016
[http://dx.doi.org/10.1155/2016/9013816]
[11]
Bryszewska, M.; Zavodnik, I.B.; Niekurzak, A.; Szosland, K. Oxidative processes in red blood cells from normal and diabetic individuals. Biochem. Mol. Biol. Int., 1995, 37(2), 345-354.
[PMID: 8673018]
[12]
Zavodnik, I.B.; Lapshina, E.A.; Rekawiecka, K.; Zavodnik, L.B.; Bartosz, G.; Bryszewska, M. Membrane effects of nitrite-induced oxidation of human red blood cells. Biochim. Biophys. Acta Biomembr., 1999, 1421(2), 306-316.
[http://dx.doi.org/10.1016/S0005-2736(99)00136-4] [PMID: 10518700]
[13]
Salama, M.F.; Abbas, A.; Darweish, M.M.; El-Hawwary, A.A.; Al-Gayyar, M.M.H. Hepatoprotective effects of cod liver oil against sodium nitrite toxicity in rats. Pharm. Biol., 2013, 51(11), 1435-1443.
[http://dx.doi.org/10.3109/13880209.2013.796564] [PMID: 23862714]
[14]
Shugaleĭ I.; L’vov, S.; Tselinskiĭ I.; Baev, V. Effect of sodium nitrite poisoning on the activity of enzymes of anti-oxidant protection and peroxidation processes in mouse erythrocytes. Ukrain Biochem. J., 1991, 64(2), 111-114.
[15]
Willett, W.C.; Koplan, J.P.; Nugent, R.; Dusenbury, C.; Puska, P.; Gaziano, T.A. Prevention of chronic disease by means of diet and lifestyle changes. In: Jamison, D.T.; Breman, J.G.; Measham, A.R.; Washington (DC): The International Bank for Reconstruction and Development/The World Bank; New York: Oxford University Press, 2006.
[16]
Xu, D.P.; Li, Y.; Meng, X.; Zhou, T.; Zhou, Y.; Zheng, J.; Zhang, J.J.; Li, H.B. Natural antioxidants in foods and medicinal plants: Extraction, assessment and resources. Int. J. Mol. Sci., 2017, 18(1), 96.
[http://dx.doi.org/10.3390/ijms18010096] [PMID: 28067795]
[17]
Preeti, S.; Prabhat, U.; Shardendu, M.; Ananya, S.; Suresh, P. Berberine a potent substance for researcher: A review. World J. Pharm. Pharm. Sci., 2015, 4, 547-573.
[18]
Jahnke, G.D.; Price, C.J.; Marr, M.C.; Myers, C.B.; George, J.D. Developmental toxicity evaluation of berberine in rats and mice. Birth Defects Res. B Dev. Reprod. Toxicol., 2006, 77(3), 195-206.
[http://dx.doi.org/10.1002/bdrb.20075] [PMID: 16634078]
[19]
Zhou, J.Y.; Zhou, S.W. Protective effect of berberine on antioxidant enzymes and positive transcription elongation factor b expression in diabetic rat liver. Fitoterapia, 2011, 82(2), 184-189.
[http://dx.doi.org/10.1016/j.fitote.2010.08.019] [PMID: 20828602]
[20]
Hwang, J.M.; Wang, C.J.; Chou, F.P.; Tseng, T.H.; Hsieh, Y.S.; Lin, W.L.; Chu, C.Y. Inhibitory effect of berberine on tert -butyl hydroperoxide-induced oxidative damage in rat liver. Arch. Toxicol., 2002, 76(11), 664-670.
[http://dx.doi.org/10.1007/s00204-002-0351-9] [PMID: 12415430]
[21]
Akhzari, M.; Shafiee, S.M.; Rashno, S.; Akmali, M. Berberine attenuated oxidative stress induced by sodium nitrite in rat liver. Jundishapur J. Nat. Pharm. Prod., 2019. In Press
[http://dx.doi.org/10.5812/jjnpp.68532]
[22]
Zhang, B.J.; Xu, D.; Guo, Y.; Ping, J.; Chen, L.; Wang, H. Protection by and anti-oxidant mechanism of berberine against rat liver fibrosis induced by multiple hepatotoxic factors. Clin. Exp. Pharmacol. Physiol., 2008, 35(3), 303-309.
[http://dx.doi.org/10.1111/j.1440-1681.2007.04819.x] [PMID: 17973934]
[23]
Albus, U. Guide for the care and use of laboratory animals, 8th ed; SAGE Publications Sage UK: London, England, 2012, pp. 267-268.
[24]
Feng, Y.; Siu, K.Y.; Ye, X.; Wang, N.; Yuen, M.F.; Leung, C.H.; Tong, Y.; Kobayashi, S. Hepatoprotective effects of berberine on carbon tetrachloride-induced acute hepatotoxicity in rats. Chin. Med., 2010, 5(1), 33.
[http://dx.doi.org/10.1186/1749-8546-5-33] [PMID: 20849653]
[25]
Hasanein, P.; Ghafari-Vahed, M.; Khodadadi, I. Effects of isoquinoline alkaloid berberine on lipid peroxidation, antioxidant defense system, and liver damage induced by lead acetate in rats. Redox Rep., 2017, 22(1), 42-50.
[http://dx.doi.org/10.1080/13510002.2016.1140406] [PMID: 26871196]
[26]
Sherif, I.O.; Al-Gayyar, M.M.H. Antioxidant, anti-inflammatory and hepatoprotective effects of silymarin on hepatic dysfunction induced by sodium nitrite. Eur. Cytokine Netw., 2013, 24(3), 114-121.
[http://dx.doi.org/10.1684/ecn.2013.0341] [PMID: 24225033]
[27]
Zhao, X.; Zhang, J.; Tong, N.; Chen, Y.; Luo, Y. Protective effects of berberine on doxorubicin-induced hepatotoxicity in mice. Biol. Pharm. Bull., 2012, 35(5), 796-800.
[http://dx.doi.org/10.1248/bpb.35.796] [PMID: 22687420]
[28]
Zeb, A.; Ullah, F. A simple spectrophotometric method for the determination of thiobarbituric acid reactive substances in fried fast foods. J. Anal. Methods Chem., 2016, 2016, 9412767.
[http://dx.doi.org/10.1155/2016/9412767]
[29]
Rahman, I.; Kode, A.; Biswas, S.K. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc., 2006, 1(6), 3159-3165.
[http://dx.doi.org/10.1038/nprot.2006.378] [PMID: 17406579]
[30]
Fecondo, J.V.; Augusteyn, R.C. Superoxide dismutase, catalase and glutathione peroxidase in the human cataractous lens. Exp. Eye Res., 1983, 36(1), 15-23.
[http://dx.doi.org/10.1016/0014-4835(83)90085-4] [PMID: 6825728]
[31]
Racker, E. Glutathione reductase from bakers’ yeast and beef liver. J. Biol. Chem., 1955, 217(2), 855-865.
[http://dx.doi.org/10.1016/S0021-9258(18)65950-2] [PMID: 13271446]
[32]
Maheshwari, D.T.; Yogendra Kumar, M.S.; Verma, S.K.; Singh, V.K.; Singh, S.N. Antioxidant and hepatoprotective activities of phenolic rich fraction of Seabuckthorn (Hippophae rhamnoides L.) leaves. Food Chem. Toxicol., 2011, 49(9), 2422-2428.
[http://dx.doi.org/10.1016/j.fct.2011.06.061] [PMID: 21723907]
[33]
Misra, H.P.; Fridovich, I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem., 1972, 247(10), 3170-3175.
[http://dx.doi.org/10.1016/S0021-9258(19)45228-9] [PMID: 4623845]
[34]
Ansari, F.A.; Mahmood, R. Sodium nitrate induces reactive oxygen species that lower the antioxidant power, damage the membrane, and alter pathways of glucose metabolism in human erythrocytes. J. Agric. Food Chem., 2015, 63(48), 10372-10379.
[http://dx.doi.org/10.1021/acs.jafc.5b04898] [PMID: 26586154]
[35]
Uslu, H.; Uslu, G.; Makav, M.; Adali, Y.; Gelen, V. Protective effects of melatonin against chronic sodium nitrite exposure in rats. Firat Univ. Saglik Bilim. Vet. Derg., 2019, 33(3), 139-145.
[36]
Al-Gayyar, M.M.H.; Al Youssef, A.; Sherif, I.O.; Shams, M.E.E.; Abbas, A. Protective effects of arjunolic acid against cardiac toxicity induced by oral sodium nitrite: Effects on cytokine balance and apoptosis. Life Sci., 2014, 111(1-2), 18-26.
[http://dx.doi.org/10.1016/j.lfs.2014.07.002] [PMID: 25064822]
[37]
Ansari, F.A.; Ali, S.N.; Mahmood, R. Sodium nitrite-induced oxidative stress causes membrane damage, protein oxidation, lipid peroxidation and alters major metabolic pathways in human erythrocytes. Toxicol. In Vitro, 2015, 29(7), 1878-1886.
[http://dx.doi.org/10.1016/j.tiv.2015.07.022] [PMID: 26231821]
[38]
Bensoltane, S.; Messerer, L.; Youbi, M.; Houria, B.; Djekoun, M. Effects of acute and sub-chronic ammonium nitrate exposure on rat liver and blood tissues. Afr. J. Biotechnol., 2006, 5(9)
[39]
Forman, H.J.; Zhang, H. Targeting oxidative stress in disease: Promise and limitations of antioxidant therapy. Nat. Rev. Drug Discov., 2021, 20(9), 689-709.
[http://dx.doi.org/10.1038/s41573-021-00233-1] [PMID: 34194012]
[40]
Pacher, P.; Beckman, J.S.; Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev., 2007, 87(1), 315-424.
[http://dx.doi.org/10.1152/physrev.00029.2006] [PMID: 17237348]
[41]
Beckman, J.S.; Koppenol, W.H. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am. J. Physiol. Cell Physiol., 1996, 271(5), C1424-C1437.
[http://dx.doi.org/10.1152/ajpcell.1996.271.5.C1424] [PMID: 8944624]
[42]
Bartsch, H.; Hietanen, E.; Malaveille, C. Carcinogenic nitrosamines: Free radical aspects of their action. Free Radic. Biol. Med., 1989, 7(6), 637-644.
[http://dx.doi.org/10.1016/0891-5849(89)90144-5] [PMID: 2695407]
[43]
Choi, S.Y.; Chung, M.J.; Sung, N.J. Volatile N-nitrosamine inhibition after intake Korean green tea and Maesil (Prunus mume SIEB. et ZACC.) extracts with an amine-rich diet in subjects ingesting nitrate. Food Chem. Toxicol., 2002, 40(7), 949-957.
[http://dx.doi.org/10.1016/S0278-6915(02)00025-X] [PMID: 12065217]
[44]
Luo, A.; Fan, Y. Antioxidant activities of berberine hydrochloride. J. Med. Plants Res., 2011, 5(16), 3702-3707.
[45]
Ye, M.; Fu, S.; Pi, R.; He, F. Neuropharmacological and pharmacokinetic properties of berberine: A review of recent research. J. Pharm. Pharmacol., 2010, 61(7), 831-837.
[http://dx.doi.org/10.1211/jpp.61.07.0001] [PMID: 19589224]
[46]
Domitrović R.; Jakovac, H.; Blagojević G. Hepatoprotective activity of berberine is mediated by inhibition of TNF-α COX-2, and iNOS expression in CCl4-intoxicated mice. Toxicology, 2011, 280(1-2), 33-43.
[http://dx.doi.org/10.1016/j.tox.2010.11.005] [PMID: 21095217]
[47]
Janbaz, K.H.; Gilani, A.H. Studies on preventive and curative effects of berberine on chemical-induced hepatotoxicity in rodents. Fitoterapia, 2000, 71(1), 25-33.
[http://dx.doi.org/10.1016/S0367-326X(99)00098-2] [PMID: 11449466]
[48]
Rad, S.Z.K.; Rameshrad, M.; Hosseinzadeh, H. Toxicology effects of Berberis vulgaris (barberry) and its active constituent, berberine: A review. Iran. J. Basic Med. Sci., 2017, 20(5), 516-529.
[PMID: 28656087]
[49]
Gardner, Z.; McGuffin, M. American Herbal Products Association’s Botanical Safety Handbook, 2nd ed; CRC Press: New York, 2013, pp. 130-132.
[50]
Kheir, M.M.; Wang, Y.; Hua, L.; Hu, J.; Li, L.; Lei, F.; Du, L. Acute toxicity of berberine and its correlation with the blood concentration in mice. Food Chem. Toxicol., 2010, 48(4), 1105-1110.
[http://dx.doi.org/10.1016/j.fct.2010.01.033] [PMID: 20138204]
[51]
Küpeli, E. Koşar, M.; Yeşilada, E.; Başer, K.H.C.; Başer, C. A comparative study on the anti-inflammatory, antinociceptive and antipyretic effects of isoquinoline alkaloids from the roots of Turkish Berberis species. Life Sci., 2002, 72(6), 645-657.
[http://dx.doi.org/10.1016/S0024-3205(02)02200-2] [PMID: 12467905]
[52]
Yeşilada, E.; Küpeli, E. Berberis crataegina DC. root exhibits potent anti-inflammatory, analgesic and febrifuge effects in mice and rats. J. Ethnopharmacol., 2002, 79(2), 237-248.
[http://dx.doi.org/10.1016/S0378-8741(01)00387-7] [PMID: 11801387]
[53]
Eaton, D.L.; Gilbert, S.G. Toxicology the basic science of poisons, 8; MC Grow Hi education: New York , 2013; pp. 34-37.
[54]
Ning, N.; Wang, Y.Z.; Zou, Z.Y.; Zhang, D.Z.; Wang, D.Z.; Li, X.G. Pharmacological and safety evaluation of fibrous root of Rhizoma Coptidis. Environ. Toxicol. Pharmacol., 2015, 39(1), 53-69.
[http://dx.doi.org/10.1016/j.etap.2014.11.006] [PMID: 25434762]
[55]
Zhou, J.Y.; Zhou, S.W.; Zhang, K.B.; Tang, J.L.; Guang, L.X.; Ying, Y.; Xu, Y.; Zhang, L.; Li, D.D. Chronic effects of berberine on blood, liver glucolipid metabolism and liver PPARs expression in diabetic hyperlipidemic rats. Biol. Pharm. Bull., 2008, 31(6), 1169-1176.
[http://dx.doi.org/10.1248/bpb.31.1169] [PMID: 18520050]

Rights & Permissions Print Cite
Article Metrics
24
2
© 2024 Bentham Science Publishers | Privacy Policy