Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Freeze-Dried Powder of Rubus coreanus Miquel Ameliorates Isoproterenol-Induced Oxidative Stress and Tissue Damage in Rats

  • Kim, Jin Tae (Department of Food Science and Biotechnology, Chung-Ang University) ;
  • Qiu, Shuai (Department of Food Science and Biotechnology, Chung-Ang University) ;
  • Zhou, Yimeng (Department of Food Science and Biotechnology, Chung-Ang University) ;
  • Moon, Ji Hyun (Department of Food Science and Biotechnology, Chung-Ang University) ;
  • Lee, Seung Beom (Department of Food Science and Biotechnology, Chung-Ang University) ;
  • Park, Ho Jin (Department of Food Science and Biotechnology, Chung-Ang University) ;
  • Lee, Hong Jin (Department of Food Science and Biotechnology, Chung-Ang University)
  • Received : 2021.06.16
  • Accepted : 2021.06.29
  • Published : 2021.09.28
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Abstract

Rubus coreanus Miquel (bokbunja), Korean black raspberry, is known to possess various phytochemicals that exert antioxidative, anti-inflammatory, and anti-cancer effects. However, most studies on Rubus coreanus Miquel have been performed with the solvent extracts and/or a single component to demonstrate the efficacy, while studies evaluating the effect of the whole fructus of Rubus coreanus Miquel are limited. In this study, therefore, we employed the isoproterenol (IPN)-induced myocardial infarction model and investigated the effect of freeze-dried powder of Rubus coreanus Miquel (RCP) on oxidative stress and prevention of organ damage. Oral administration of RCP reduced the level of toxicity markers, alanine transaminase (ALT), aspartate transaminase (AST), and lactate dehydrogenase (LDH) without affecting body weight and diet intake. The oxidative stress marker glutathione (GSH) increased about 45% and malonaldehyde (MDA) decreased about 27% compared to the IPN group with RCP-H (3%) administration. By histological analysis, IPN induced significant myocardial damage in the heart and vascular injury in the liver, and RCP administration ameliorated the damages in a dose-dependent manner. Taken together, RCP activated the antioxidant system leading to prevention of damage to organs by IPN in rats, making it possible to expect beneficial efficacies by consuming the whole fructus of Rubus coreanus Miquel.

Keywords

Acknowledgement

This research was supported by '2020 Discovering Functional Crops Project' of The Food Industry Promotional Agency of Korea and by the Chung-Ang University Research Scholarship Grants in 2020.

References

  1. Park JH, Oh SM, Lim SS, Lee YS, Shin HK, Oh YS, et al. 2006. Induction of heme oxygenase-1 mediates the anti-inflammatory effects of the ethanol extract of Rubus coreanus in murine macrophages. Biochem. Biophys. Res. Commun. 351: 146-152. https://doi.org/10.1016/j.bbrc.2006.10.008
  2. Lee JE, Cho SM, Park E, Lee SM, Kim Y, Auh JH, et al. 2014. Anti-inflammatory effects of Rubus coreanus miquel through inhibition of NF-kappaB and MAP Kinase. Nutr. Res. Pract. 8: 501-508. https://doi.org/10.4162/nrp.2014.8.5.501
  3. Bhandary B, Lee GH, Marahatta A, Lee HY, Kim SY, So BO, et al. 2012. Water extracts of immature Rubus coreanus regulate lipid metabolism in liver cells. Biol. Pharm. Bull. 35: 1907-1913. https://doi.org/10.1248/bpb.b12-00022
  4. Lee KH, Jeong ES, Jang G, Na JR, Park S, Kang WS, et al. 2020. Unripe Rubus coreanus miquel extract containing ellagic acid regulates AMPK, SREBP-2, HMGCR, and INSIG-1 signaling and cholesterol metabolism in vitro and in vivo. Nutrients 12: 610. https://doi.org/10.3390/nu12030610
  5. Do SH, Lee JW, Jeong WI, Chung JY, Park SJ, Hong IH, et al. 2008. Bone-protecting effect of Rubus coreanus by dual regulation of osteoblasts and osteoclasts. Menopause 15: 676-683. https://doi.org/10.1097/gme.0b013e31815bb687
  6. Kim KJ, Jeong ES, Lee KH, Na JR, Park S, Kim JS, et al. 2020. Unripe Rubus coreanus miquel extract containing ellagic acid promotes lipolysis and thermogenesis in vitro and in vivo. Molecules 25: 5954. https://doi.org/10.3390/molecules25245954
  7. Kim Y, Lee SM, Kim JH. 2014. Unripe Rubus coreanus miquel suppresses migration and invasion of human prostate cancer cells by reducing matrix metalloproteinase expression. Biosci. Biotechnol. Biochem. 78: 1402-1411. https://doi.org/10.1080/09168451.2014.921550
  8. Ko SH, Chol SW, Ye SK, Yoo S, Kim HS, Chung MH. 2008. Comparison of anti-oxidant activities of seventy herbs that have been used in Korean traditional medicine. Nutr. Res. Pract. 2: 143-151. https://doi.org/10.4162/nrp.2008.2.3.143
  9. Davel AP, Brum PC, Rossoni LV. 2014. Isoproterenol induces vascular oxidative stress and endothelial dysfunction via a Gialpha-coupled beta2-adrenoceptor signaling pathway. PLoS One 9: e91877. https://doi.org/10.1371/journal.pone.0091877
  10. Srivastava S, Chandrasekar B, Gu Y, Luo J, Hamid T, Hill BG, et al. 2007. Downregulation of CuZn-superoxide dismutase contributes to beta-adrenergic receptor-mediated oxidative stress in the heart. Cardiovasc. Res. 74: 445-455. https://doi.org/10.1016/j.cardiores.2007.02.016
  11. Rathore N, John S, Kale M, Bhatnagar D. 1998. Lipid peroxidation and antioxidant enzymes in isoproterenol induced oxidative stress in rat tissues. Pharmacol. Res. 38: 297-303. https://doi.org/10.1006/phrs.1998.0365
  12. Manjula TS, Devi CS. 1993. Effect of aspirin on isoproterenol induced changes in lipid metabolism in rats. Indian J. Med. Res. 98: 30-33.
  13. Tayeb W, Nakbi A, Cheraief I, Miled A, Hammami M. 2013. Alteration of lipid status and lipid metabolism, induction of oxidative stress and lipid peroxidation by 2,4-dichlorophenoxyacetic herbicide in rat liver. Toxicol. Mech. Methods 23: 449-458. https://doi.org/10.3109/15376516.2013.780275
  14. Pandey KB, Rizvi SI. 2009. Plant polyphenols as dietary antioxidants in human health and disease. Oxid. Med. Cell. Longev. 2: 270-278. https://doi.org/10.4161/oxim.2.5.9498
  15. Kannan MM, Quine SD. 2011. Ellagic acid ameliorates isoproterenol induced oxidative stress: evidence from electrocardiological, biochemical and histological study. Eur. J. Pharmacol. 659: 45-52. https://doi.org/10.1016/j.ejphar.2011.02.037
  16. Yeager JC, Iams SG. 1981. The hemodynamics of isoproterenol-induced cardiac failure in the rat. Circ. Shock 8: 151-163.
  17. Upaganlawar A, Gandhi C, Balaraman R. 2009. Effect of green tea and Vitamin E combination in isoproterenol induced myocardial infarction in rats. Plant Foods Hum. Nutr. 64: 75-80. https://doi.org/10.1007/s11130-008-0105-9
  18. Laine GA, Allen SJ. 1991. Left ventricular myocardial edema. Lymph flow, interstitial fibrosis, and cardiac function. Circ. Res. 68: 1713-1721. https://doi.org/10.1161/01.RES.68.6.1713
  19. Judd JT, Wexler BC. 1974. Myocardial glycoprotein changes with isoproterenol-induced necrosis and repair in the rat. Am. J. Physiol. 226: 597-602. https://doi.org/10.1152/ajplegacy.1974.226.3.597
  20. Sabeena Farvin KH, Anandan R, Kumar SH, Shiny KS, Sankar TV, Thankappan TK. 2004. Effect of squalene on tissue defense system in isoproterenol-induced myocardial infarction in rats. Pharmacol. Res. 50: 231-236. https://doi.org/10.1016/j.phrs.2004.03.004
  21. Chae HJ, Yim JE, Kim KA, Chyun JH. 2014. Hepatoprotective effects of Rubus coreanus miquel concentrates on liver injuries induced by carbon tetrachloride in rats. Nutr. Res. Pract. 8: 40-45. https://doi.org/10.4162/nrp.2014.8.1.40
  22. Nardi GM, Farias Januario AG, Freire CG, Megiolaro F, Schneider K, Perazzoli MR, et al. 2016. Anti-inflammatory activity of berry fruits in mice model of inflammation is based on oxidative stress modulation. Pharmacognosy Res. 8: S42-49. https://doi.org/10.4103/0974-8490.178642
  23. Forni C, Facchiano F, Bartoli M, Pieretti S, Facchiano A, D'Arcangelo D, et al. 2019. Beneficial role of phytochemicals on oxidative stress and age-related diseases. Biomed. Res. Int. 2019: 8748253.
  24. Hasan R, Lasker S, Hasan A, Zerin F, Zamila M, Chowdhury FI, et al. 2020. Canagliflozin attenuates isoprenaline-induced cardiac oxidative stress by stimulating multiple antioxidant and anti-inflammatory signaling pathways. Sci. Rep. 10: 14459. https://doi.org/10.1038/s41598-020-71449-1
  25. Marrocco I, Altieri F, Peluso I. 2017. Measurement and clinical significance of biomarkers of oxidative stress in humans. Oxid. Med. Cell. Longev. 2017: 6501046. https://doi.org/10.1155/2017/6501046
  26. Mohamadin AM, Elberry AA, Mariee AD, Morsy GM, Al-Abbasi FA. 2012. Lycopene attenuates oxidative stress and heart lysosomal damage in isoproterenol induced cardiotoxicity in rats: a biochemical study. Pathophysiology 19: 121-130. https://doi.org/10.1016/j.pathophys.2012.04.005
  27. Chen W, Liang J, Fu Y, Jin Y, Yan R, Chi J, et al. 2020. Cardioprotection of cortistatin against isoproterenol-induced myocardial injury in rats. Ann. Transl. Med. 8: 309. https://doi.org/10.21037/atm.2020.02.93
  28. Zhang GX, Kimura S, Nishiyama A, Shokoji T, Rahman M, Yao L, et al. 2005. Cardiac oxidative stress in acute and chronic isoproterenol-infused rats. Cardiovasc. Res. 65: 230-238. https://doi.org/10.1016/j.cardiores.2004.08.013
  29. Blasig IE, Blasig R, Lowe H. 1984. Myocardial lipid peroxidation during isoproterenol-induced blood flow reduction in rat myocardium. Biomed. Biochim. Acta 43: S171-174.
  30. Zhou R, Xu Q, Zheng P, Yan L, Zheng J, Dai G. 2008. Cardioprotective effect of fluvastatin on isoproterenol-induced myocardial infarction in rat. Eur. J. Pharmacol. 586: 244-250. https://doi.org/10.1016/j.ejphar.2008.02.057
  31. Wang SB, Tian S, Yang F, Yang HG, Yang XY, Du GH. 2009. Cardioprotective effect of salvianolic acid A on isoproterenol-induced myocardial infarction in rats. Eur. J. Pharmacol. 615: 125-132. https://doi.org/10.1016/j.ejphar.2009.04.061
  32. Yogeeta SK, Hanumantra RB, Gnanapragasam A, Senthilkumar S, Subhashini R, Devaki T. 2006. Attenuation of abnormalities in the lipid metabolism during experimental myocardial infarction induced by isoproterenol in rats: beneficial effect of ferulic acid and ascorbic acid. Basic Clin. Pharmacol. Toxicol. 98: 467-472. https://doi.org/10.1111/j.1742-7843.2006.pto_335.x
  33. Rajadurai M, Stanely Mainzen Prince P. 2006. Preventive effect of naringin on lipids, lipoproteins and lipid metabolic enzymes in isoproterenol-induced myocardial infarction in Wistar rats. J. Biochem. Mol. Toxicol. 20: 191-197. https://doi.org/10.1002/jbt.20136
  34. Tosheska Trajkovska K, Topuzovska S. 2017. High-density lipoprotein metabolism and reverse cholesterol transport: strategies for raising HDL cholesterol. Anatol. J. Cardiol. 18: 149-154.
  35. Feng CC, Liao PH, Tsai HI, Cheng SM, Yang LY, PadmaViswanadha V, et al. 2018. Tumorous imaginal disc 1 (TID1) inhibits isoproterenol-induced cardiac hypertrophy and apoptosis by regulating c-terminus of hsc70-interacting protein (CHIP) mediated degradation of Galphas. Int. J. Med. Sci. 15: 1537-1546. https://doi.org/10.7150/ijms.24296
  36. Selvaraj P, Pugalendi KV. 2012. Efficacy of hesperidin on plasma, heart and liver tissue lipids in rats subjected to isoproterenol-induced cardiotoxicity. Exp. Toxicol. Pathol. 64: 449-452. https://doi.org/10.1016/j.etp.2010.10.012
  37. Devika PT, Stanely Mainzen Prince P. 2008. (-)Epigallocatechin-gallate (EGCG) prevents mitochondrial damage in isoproterenol-induced cardiac toxicity in albino Wistar rats: a transmission electron microscopic and in vitro study. Pharmacol. Res. 57: 351-357. https://doi.org/10.1016/j.phrs.2008.03.008
  38. Garg S, Malhotra RK, Khan SI, Sarkar S, Susrutha PN, Singh V, et al. 2019. Fisetin attenuates isoproterenol-induced cardiac ischemic injury in vivo by suppressing RAGE/NF-kappaB mediated oxidative stress, apoptosis and inflammation. Phytomedicine 56: 147-155. https://doi.org/10.1016/j.phymed.2018.09.187
  39. Teng H, Lin Q, Li K, Yuan B, Song H, Peng H, et al. 2017. Hepatoprotective effects of raspberry (Rubus coreanus miq.) seed oil and its major constituents. Food Chem. Toxicol. 110: 418-424. https://doi.org/10.1016/j.fct.2017.09.010
  40. Yang JW, Choi IS. 2016. Comparison of the phenolic composition and antioxidant activity of Korean black raspberry, Bokbunja, (Rubus coreanus miquel) with those of six other berries. CYTA - J. Food 15: 110-117.