Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Implications of red Panax ginseng in oxidative stress associated chronic diseases

  • Lee, Yoon-Mi (Division of Food Bioscience, College of Biomedical and Health Sciences, Konkuk University) ;
  • Yoon, Haelim (Division of Food Bioscience, College of Biomedical and Health Sciences, Konkuk University) ;
  • Park, Hyun-Min (Division of Food Bioscience, College of Biomedical and Health Sciences, Konkuk University) ;
  • Song, Byeng Chun (Division of Food Bioscience, College of Biomedical and Health Sciences, Konkuk University) ;
  • Yeum, Kyung-Jin (Division of Food Bioscience, College of Biomedical and Health Sciences, Konkuk University)
  • Received : 2015.12.14
  • Accepted : 2016.03.04
  • Published : 2017.04.15
Download PDF
⟨ Previous Next ⟩

Abstract

The steaming process of Panax ginseng has been reported to increase its major known bioactive components, ginsenosides, and, therefore, its biological properties as compared to regular Panax ginseng. Biological functions of red Panax ginseng attenuating pro-oxidant environments associated with chronic diseases are of particular interest, since oxidative stress can be a key contributor to the pathogenesis of chronic diseases. Additionally, proper utilization of various biomarkers for evaluating antioxidant activities in natural products, such as ginseng, can also be important to providing validity to their activities. Thus, studies on the effects of red ginseng against various diseases as determined in cell lines, animal models, and humans were reviewed, along with applied biomarkers for verifying such effects. Limitations and future considerations of studying red ginseng were been discussed. Although further clinical studies are warranted, red ginseng appears to be beneficial for attenuating disease-associated symptoms via its antioxidant activities, as well as for preventing oxidative stress-associated chronic diseases.

Keywords

References

  1. Radad K, Gille G, Liu L, Rausch WD. Use of ginseng in medicine with emphasis on neurodegenerative disorders. J Pharmacol Sci 2006;100:175-86. https://doi.org/10.1254/jphs.CRJ05010X
  2. Bae JS, Park HS, Park JW, Li SH, Chun YS. Red ginseng and 20(S)-Rg3 control testosterone-induced prostate hyperplasia by deregulating androgen receptor signaling. J Nat Med 2012;66:476-85. https://doi.org/10.1007/s11418-011-0609-8
  3. Choi YJ, Choi H, Cho CH, Park JW. Red ginseng deregulates hypoxia-induced genes by dissociating the HIF-1 dimer. J Nat Med 2011;65:344-52. https://doi.org/10.1007/s11418-010-0504-8
  4. Helms S. Cancer prevention and therapeutics: Panax ginseng. Altern Med Rev 2004;9:259-74.
  5. Wong VK, Cheung S, Li T, Jiang ZH, Wang JR, Dong H, Yi XQ, Zhou H, Liu L. Asian ginseng extract inhibits in vitro and in vivo growth of mouse lewis lung carcinoma via modulation of ERK-p53 and NF-kappaB signaling. J Cell Biochem 2010;111:899-910. https://doi.org/10.1002/jcb.22778
  6. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009;8:579-91. https://doi.org/10.1038/nrd2803
  7. Chen K, Gunter K, Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem 2000;75:304-13.
  8. Khansari N, Shakiba Y, Mahmoudi M. Chronic inflammation and oxidative stress as a major cause of age-related diseases and cancer. Recent Pat Inflamm Allergy Drug Discov 2009;3:73-80. https://doi.org/10.2174/187221309787158371
  9. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 2011;1:7-15.
  10. Curtin JF, Donovan M, Cotter TG. Regulation and measurement of oxidative stress in apoptosis. J Immunol Methods 2002;265:49-72. https://doi.org/10.1016/S0022-1759(02)00070-4
  11. Wu LL, Chiou CC, Chang PY, Wu JT. Urinary 8-OHdG: a marker of oxidative stress to DNA and a risk factor for cancer, atherosclerosis and diabetics. Clinica Chimica Acta 2004;339:1-9. https://doi.org/10.1016/j.cccn.2003.09.010
  12. Sharma A, Singh K, Almasan A. Histone H2AX phosphorylation: a marker for DNA damage. Methods Mol Biol 2012;920:613-26.
  13. Kuo LJ, Yang LX. Gamma-H2AX - a novel biomarker for DNA double-strand breaks. Vivo 2008;22:305-9.
  14. Olive PL, Banath JP. The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 2006;1:23-9. https://doi.org/10.1038/nprot.2006.5
  15. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, Guldberg P, Sehested M, Nesland JM, Lukas C, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005;434:864-70. https://doi.org/10.1038/nature03482
  16. Ho E, Karimi Galougahi K, Liu CC, Bhindi R, Figtree GA. Biological markers of oxidative stress: applications to cardiovascular research and practice. Redox Biol 2013;1:483-91. https://doi.org/10.1016/j.redox.2013.07.006
  17. Meagher EA, FitzGerald GA. Indices of lipid peroxidation in vivo: strengths and limitations. Free Radic Biol Med 2000;28:1745-70. https://doi.org/10.1016/S0891-5849(00)00232-X
  18. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 2003;53:S26-33. https://doi.org/10.1002/ana.10483
  19. Rahman I, van Schadewijk AA, Crowther AJ, Hiemstra PS, Stolk J, MacNee W, De Boer WI. 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002;166:490-5. https://doi.org/10.1164/rccm.2110101
  20. Song BC, Joo NS, Aldini G, Yeum KJ. Biological functions of histidine-dipeptides and metabolic syndrome. Nutr Res Pract 2014;8:3-10. https://doi.org/10.4162/nrp.2014.8.1.3
  21. Kim YK, Guo Q, Packer L. Free radical scavenging activity of red ginseng aqueous extracts. Toxicology 2002;172:149-56. https://doi.org/10.1016/S0300-483X(01)00585-6
  22. Park BJ, Lim YS, Lee HJ, Eum WS, Park J, Han KH, Choi SY, Lee KS. Antioxidative effects of Phellinus linteus and red ginseng extracts on oxidative stress-induced DNA damage. BMB Rep 2009;42:500-5. https://doi.org/10.5483/BMBRep.2009.42.8.500
  23. Im GJ, Chang JW, Choi J, Chae SW, Ko EJ, Jung HH. Protective effect of Korean red ginseng extract on cisplatin ototoxicity in HEI-OC1 auditory cells. Phytother Res 2010;24:614-21.
  24. Park SH, Jang JH, Chen CY, Na HK, Surh YJ. A formulated red ginseng extract rescues PC12 cells from PCB-induced oxidative cell death through Nrf2-mediated upregulation of heme oxygenase-1 and glutamate cysteine ligase. Toxicology 2010;278:131-9. https://doi.org/10.1016/j.tox.2010.04.003
  25. Bak MJ, Jun M, Jeong WS. Antioxidant and hepatoprotective effects of the red ginseng essential oil in H(2)O(2)-treated hepG2 cells and CCl(4)-treated mice. Int J Mol Sci 2012;13:2314-30. https://doi.org/10.3390/ijms13022314
  26. Park HM, Kim SJ, Mun AR, Go HK, Kim GB, Kim SZ, Jang SI, Lee SJ, Kim JS, Kang HS. Korean red ginseng and its primary ginsenosides inhibit ethanolinduced oxidative injury by suppression of the MAPK pathway in TIB-73 cell. J Ethnopharmacol 2012;141:1071-6. https://doi.org/10.1016/j.jep.2012.03.038
  27. Sohn SH, Kim SK, Kim YO, Kim HD, Shin YS, Yang SO, Kim SY, Lee SW. A comparison of antioxidant activity of Korean White and Red Ginsengs on $H_2O_2$-induced oxidative stress in HepG2 hepatoma cells. J Ginseng Res 2013;37:442-50. https://doi.org/10.5142/jgr.2013.37.442
  28. Dong GZ, Jang EJ, Kang SH, Cho IJ, Park SD, Kim SC, Kim YW. Red ginseng abrogates oxidative stress via mitochondria protection mediated by LKB1-AMPK pathway. BMC Complement Altern Med 2013;13:64. https://doi.org/10.1186/1472-6882-13-64
  29. Kim S, Lee Y, Cho J. Korean red ginseng extract exhibits neuroprotective effects through inhibition of apoptotic cell death. Biol Pharm Bull 2014;37:938-46. https://doi.org/10.1248/bpb.b13-00880
  30. Han JY, Ahn SY, Oh EH, Nam SY, Hong JT, Oh KW, Lee MK. Red ginseng extract attenuates kainate-induced excitotoxicity by antioxidative effects. Evid Based Complement Alternat Med 2012;2012:479016.
  31. Cho SO, Lim JW, Kim H. Red ginseng extract inhibits the expression of MCP-1 and iNOS in Helicobacter pylori-infected gastric epithelial cells by suppressing the activation of NADPH oxidase and Jak2/Stat3. J Ethnopharmacol 2013;150:761-4. https://doi.org/10.1016/j.jep.2013.09.013
  32. Chang JW, Park KH, Hwang HS, Shin YS, Oh YT, Kim CH. Protective effects of Korean red ginseng against radiation-induced apoptosis in human HaCaT keratinocytes. J Radiat Res 2014;55:245-6. https://doi.org/10.1093/jrr/rrt109
  33. Park HR, Lee SE, Yang H, Son GW, Jin YH, Park YS. Induction of thioredoxin reductase 1 by Korean red ginseng water extract regulates cytoprotective effects on human endothelial cells. Evid Based Complement Alternat Med 2015;2015:972040.
  34. Lee SE, Park YS. Korean Red Ginseng water extract inhibits COX-2 expression by suppressing p38 in acrolein-treated human endothelial cells. J Ginseng Res 2014;38:34-9. https://doi.org/10.1016/j.jgr.2013.11.004
  35. Kim HY, Kim K. Protective effect of ginseng on cytokine-induced apoptosis in pancreatic beta-cells. J Agric Food Chem 2007;55:2816-23. https://doi.org/10.1021/jf062577r
  36. Sahhugi Z, Hasenan SM, Jubri Z. Protective effects of gelam honey against oxidative damage in young and aged rats. Oxid Med Cell Longev 2014;2014:673628.
  37. Ramesh T, Kim SW, Hwang SY, Sohn SH, Yoo SK, Kim SK. Panax ginseng reduces oxidative stress and restores antioxidant capacity in aged rats. Nutr Res 2012;32:718-26. https://doi.org/10.1016/j.nutres.2012.08.005
  38. Kopalli SR, Hwang SY, Won YJ, Kim SW, Cha KM, Han CK, Hong JY, Kim SK. Korean red ginseng extract rejuvenates testicular ineffectiveness and sperm maturation process in aged rats by regulating redox proteins and oxidative defense mechanisms. Exp Gerontol 2015;69:94-102. https://doi.org/10.1016/j.exger.2015.05.004
  39. Park S, Kim CS, Min J, Lee SH, Jung YS. A high-fat diet increases oxidative renal injury and protein glycation in D-galactose-induced aging rats and its prevention by Korea red ginseng. J Nutr Sci Vitaminol 2014;60:159-66. https://doi.org/10.3177/jnsv.60.159
  40. Kim YS, Kim YH, Noh JR, Cho ES, Park JH, Son HY. Protective effect of Korean red ginseng against aflatoxin B1-Induced hepatotoxicity in rat. J Ginseng Res 2011;35:243-9. https://doi.org/10.5142/jgr.2011.35.2.243
  41. Han JY, Lee S, Yang JH, Kim S, Sim J, Kim MG, Jeong TC, Ku SK, Cho IJ, Ki SH. Korean Red Ginseng attenuates ethanol-induced steatosis and oxidative stress via AMPK/Sirt1 activation. J Ginseng Res 2015;39:105-15. https://doi.org/10.1016/j.jgr.2014.09.001
  42. Kim HJ, Lee SG, Chae IG, Kim MJ, Im NK, Yu MH, Lee EJ, Lee IS. Antioxidant effects of fermented red ginseng extracts in streptozotocin- induced diabetic rats. J Ginseng Res 2011;35:129-37. https://doi.org/10.5142/jgr.2011.35.2.129
  43. Lim SW, Doh KC, Jin L, Piao SG, Heo SB, Zheng YF, Bae SK, Chung BH, Yang CW. Oral administration of ginseng ameliorates cyclosporine-induced pancreatic injury in an experimental mouse model. PloS ONE 2013;8:e72685. https://doi.org/10.1371/journal.pone.0072685
  44. Oyagi A, Ogawa K, Kakino M, Hara H. Protective effects of a gastrointestinal agent containing Korean red ginseng on gastric ulcer models in mice. BMC Complement Altern Med 2010;10:45. https://doi.org/10.1186/1472-6882-10-45
  45. Yu SY, Yoon BR, Lee YJ, Lee JS, Hong HD, Lee YC, Kim YC, Cho CW, Kim KT, Lee OH. Inhibitory effect of high temperature- and high pressure-treated red ginseng on exercise-induced oxidative stress in ICR mouse. Nutrients 2014;6:1003-15. https://doi.org/10.3390/nu6031003
  46. Kim KR, Chung TY, Shin H, Son SH, Park KK, Choi JH, Chung WY. Red ginseng saponin extract attenuates murine collagen-induced arthritis by reducing pro-inflammatory responses and matrix metalloproteinase-3 expression. Biol Pharm Bill 2010;33:604-10. https://doi.org/10.1248/bpb.33.604
  47. Sharma J, Goyal PK. Chemoprevention of chemical-induced skin cancer by Panax ginseng root extract. J Ginseng Res 2015;39:265-73. https://doi.org/10.1016/j.jgr.2015.01.005
  48. Kim JY, Park JY, Kang HJ, Kim OY, Lee JH. Beneficial effects of Korean red ginseng on lymphocyte DNA damage, antioxidant enzyme activity, and LDL oxidation in healthy participants: a randomized, double-blind, placebocontrolled trial. Nutr J 2012;11:47. https://doi.org/10.1186/1475-2891-11-47
  49. Seo SK, Hong Y, Yun BH, Chon SJ, Jung YS, Park JH, Cho S, Choi YS, Lee BS. Antioxidative effects of Korean red ginseng in postmenopausal women: a double-blind randomized controlled trial. J Ethnopharmacol 2014;154:753-7. https://doi.org/10.1016/j.jep.2014.04.051
  50. Park SJ, Lim KH, Noh H, Jeong EJ, Kim YS, Han BC, Lee SH, Moon KS. Subacute oral toxicity study of Korean red ginseng extract in Sprague-Dawley rats. Toxicol Res 2013;29:285-92. https://doi.org/10.5487/TR.2013.29.4.285
  51. Bak MJ, Kim KB, Jun J, Jeong WS. Safety of red ginseng oil for single oral administration in Sprague-Dawley rats. J Ginseng Res 2014;38:78-81. https://doi.org/10.1016/j.jgr.2013.11.009
  52. Paik DJ, Lee CH. Review of cases of patient risk associated with ginseng abuse and misuse. J Ginseng Res 2015;39:89-93. https://doi.org/10.1016/j.jgr.2014.11.005
  53. Huu Tung N, Uto T, Morinaga O, Kim YH, Shoyama Y. Pharmacological effects of ginseng on liver functions and diseases: a mini review. Evid Based Complement Alternat Med 2012;2012:173297.

Cited by

  1. Gamma irradiation-induced liver injury and its amelioration by red ginseng extract vol.13, pp.4, 2017, https://doi.org/10.1007/s13273-017-0050-5
  2. Pectinase-treated Panax ginseng protects heat stress-induced testicular damage in rats vol.153, pp.6, 2017, https://doi.org/10.1530/rep-16-0560
  3. Ginsenoside Re Attenuates Isoproterenol-Induced Myocardial Injury in Rats vol.2018, pp.None, 2017, https://doi.org/10.1155/2018/8637134
  4. Multi-Target Protective Effects of Gintonin in 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-Mediated Model of Parkinson’s Disease via Lysophosphatidic Acid Receptors vol.9, pp.None, 2017, https://doi.org/10.3389/fphar.2018.00515
  5. Neuroprotective Effects of a Traditional Multi-Herbal Medicine Kyung-Ok-Ko in an Animal Model of Parkinson's Disease: Inhibition of MAPKs and NF-κB Pathways and Activation of Keap1-Nrf2 Pathway vol.9, pp.None, 2017, https://doi.org/10.3389/fphar.2018.01444
  6. Efficacy and Mechanism of Panax Ginseng in Experimental Stroke vol.13, pp.None, 2017, https://doi.org/10.3389/fnins.2019.00294
  7. Comparative study on anti-oxidative and anti-inflammatory properties of hydroponic ginseng and soil-cultured ginseng vol.28, pp.1, 2019, https://doi.org/10.1007/s10068-018-0450-x
  8. The Protective Effect of Korean Red Ginseng Against Rotenone-Induced Parkinson’s Disease in Rat Model: Modulation of Nuclear Factor-κβ and Caspase-3 vol.20, pp.7, 2017, https://doi.org/10.2174/1389201020666190611122747
  9. Phenolic Compounds and Ginsenosides in Ginseng Shoots and Their Antioxidant and Anti-Inflammatory Capacities in LPS-Induced RAW264.7 Mouse Macrophages vol.20, pp.12, 2017, https://doi.org/10.3390/ijms20122951
  10. Effects of Rhodiola rosea and Panax ginseng on the Metabolic Parameters of Rats Submitted to Swimming vol.22, pp.10, 2019, https://doi.org/10.1089/jmf.2019.0062
  11. In vitro and in silico evaluation of stereoselective effect of ginsenoside isomers on platelet P2Y12 receptor vol.64, pp.None, 2017, https://doi.org/10.1016/j.phymed.2019.152899
  12. Transcriptomic profiling reveals MEP pathway contributing to ginsenoside biosynthesis in Panax ginseng vol.20, pp.None, 2019, https://doi.org/10.1186/s12864-019-5718-x
  13. Anti-Inflammatory Potential of Cultured Ginseng Roots Extract in Lipopolysaccharide-Stimulated Mouse Macrophages and Adipocytes vol.17, pp.13, 2017, https://doi.org/10.3390/ijerph17134716
  14. Research Quality-Based Multivariate Modeling for Comparison of the Pharmacological Effects of Black and Red Ginseng vol.12, pp.9, 2017, https://doi.org/10.3390/nu12092590
  15. Effect of Korean Red Ginseng on Cholesterol Metabolites in Postmenopausal Women with Hypercholesterolemia: A Pilot Randomized Controlled Trial vol.12, pp.11, 2017, https://doi.org/10.3390/nu12113423
  16. Vitamin E and ginseng supplementation to enhance female sexual function: a randomized, double-blind, placebo-controlled, clinical trial vol.60, pp.10, 2017, https://doi.org/10.1080/03630242.2020.1803465
  17. The cardio and renoprotective role of ginseng against epinephrine-induced myocardial infarction in rats: Involvement of angiotensin II type 1 receptor/protein kinase C vol.8, pp.None, 2021, https://doi.org/10.1016/j.toxrep.2021.04.008
  18. The effects of ginseng on the metabolic syndrome: An updated review vol.9, pp.9, 2021, https://doi.org/10.1002/fsn3.2475
  19. Korean Red Ginseng Ameliorates Fatigue via Modulation of 5-HT and Corticosterone in a Sleep-Deprived Mouse Model vol.13, pp.9, 2021, https://doi.org/10.3390/nu13093121
  20. Efficacy of Panax ginseng supplementation on androgen deficiency rats via metabolomics and gut microbiota vol.87, pp.None, 2021, https://doi.org/10.1016/j.jff.2021.104810