Journal of Ginseng Research

  • 제41권4호
  • /
  • Pages.589-594
  • /
  • 2017
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  • 1226-8453(pISSN)
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  • 2093-4947(eISSN)
고려인삼학회 (The Korean Society of Ginseng)
권호 표지
DOI QR코드

DOI QR Code

Effects of ginseng on stress-related depression, anxiety, and the hypothalamic-pituitary-adrenal axis

  • 투고 : 2016.10.01
  • 심사 : 2017.01.18
  • 발행 : 2017.10.15
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⟨ 이전 논문 다음 논문 ⟩

초록

Ginseng effectively regulates the immune response and the hormonal changes due to stress, thus maintaining homeostasis. In addition to suppressing the occurrence of psychological diseases such as anxiety and depression, ginseng also prevents stress-associated physiological diseases. Recent findings have revealed that ginseng is involved in adjusting the hypothalamic-pituitary-adrenal axis and controlling hormones, thus producing beneficial effects on the heart and brain, and in cases of bone diseases, as well as alleviating erectile dysfunction. Recent studies have highlighted the potential use of ginseng in the prevention and treatment of chronic inflammatory diseases such as diabetes, rheumatoid arthritis, and allergic asthma. However, the mechanism underlying the effects of ginseng on these stress-related diseases has not been completely established. In this review, we focus on the disease pathways caused by stress in order to determine how ginseng acts to improve health. Central to our discussion is how this effective and stable therapeutic agent alleviates the anxiety and depression caused by stress and ameliorates inflammatory diseases.

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참고문헌

  1. Le Fevre M, Matheny J, Kolt GS. Eustress, distress, and interpretation in occupational stress. J Managerial Psychol 2003;18:726-44. https://doi.org/10.1108/02683940310502412
  2. Attele AS, Wu JA, Yuan CS. Ginseng pharmacology: multiple constituents and multiple actions. Biochem Pharmacol 1999;58:1685-93. https://doi.org/10.1016/S0006-2952(99)00212-9
  3. Choi HK, Seong DH, Rha KH. Clinical efficacy of Korean red ginseng for erectile dysfunction. Int J Impot Res 1995;7:181-6.
  4. Kim DH. Chemical diversity of Panax ginseng, Panax quinquifolium, and Panax notoginseng. J Ginseng Res 2012;36:1-15. https://doi.org/10.5142/jgr.2012.36.1.1
  5. Nah SY, Kim DH, Rhim H. Ginsenosides: are any of them candidates for drugs acting on the central nervous system? CNS Drug Rev 2007;13:381-404.
  6. Helms S. Cancer prevention and therapeutics: Panax ginseng. Altern Med Rev 2004;9:259-74.
  7. Nguyen CT, Luong TT, Lee SY, Kim GL, Kwon H, Lee HG, Park CK, Rhee DK. Panax ginseng aqueous extract prevents pneumococcal sepsis in vivo by potentiating cell survival and diminishing inflammation. Phytomedicine 2015;22:1055-61. https://doi.org/10.1016/j.phymed.2015.07.005
  8. Liao B, Newmark H, Zhou R. Neuroprotective effects of ginseng total saponin and ginsenosides Rb1 and Rg1 on spinal cord neurons in vitro. Exp Neurol 2002;173:224-34. https://doi.org/10.1006/exnr.2001.7841
  9. Lee E, Kim S, Chung KC, Choo MK, Kim DH, Nam G, Rhim H. 20(S)-Ginsenoside Rh2, a newly identified active ingredient of ginseng, inhibits NMDA receptors in cultured rat hippocampal neurons. Eur J Pharmacol 2006;536:69-77. https://doi.org/10.1016/j.ejphar.2006.02.038
  10. Thatte U, Bagadey S, Dahanukar S. Modulation of programmed cell death by medicinal plants. Cell Mol Biol 2000;46:199-214.
  11. Hasegawa H. Proof of the mysterious efficacy of ginseng: basic and clinical trials: metabolic activation of ginsenoside: deglycosylation by intestinal bacteria and esterification with fatty acid. J Pharmacol Sci 2004;95:153-7. https://doi.org/10.1254/jphs.FMJ04001X4
  12. Leung KW, Yung KK, Mak NK, Chan YS, Fan TP, Wong RN. Neuroprotective effects of ginsenoside-Rg1 in primary nigral neurons against rotenone toxicity. Neuropharmacology 2007;52:827-35. https://doi.org/10.1016/j.neuropharm.2006.10.001
  13. Rege NN, Thatte UM, Dahanukar SA. Adaptogenic properties of six rasayana herbs used in Ayurvedic medicine. Phytother Res 1999;13:275-91. https://doi.org/10.1002/(SICI)1099-1573(199906)13:4<275::AID-PTR510>3.0.CO;2-S
  14. Kim EH, Kim IH, Lee MJ, Thach Nguyen C, Ha JA, Lee SC, Choi S, Choi KT, Pyo S, Rhee DK. Anti-oxidative stress effect of red ginseng in the brain is mediated by peptidyl arginine deiminase type IV (PADI4) repression via estrogen receptor (ER) beta up-regulation. J Ethnopharmacol 2013;148:474-85. https://doi.org/10.1016/j.jep.2013.04.041
  15. Dang H, Chen Y, Liu X, Wang Q, Wang L, Jia W, Wang Y. Antidepressant effects of ginseng total saponins in the forced swimming test and chronic mild stress models of depression. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:1417-24. https://doi.org/10.1016/j.pnpbp.2009.07.020
  16. Guilliams TG, Edwards L. Chronic stress and the HPA axis. The Standard 2010;9:1-12.
  17. Tomas C, Newton J, Watson S. A review of hypothalamic-pituitary-adrenal axis function in chronic fatigue syndrome. ISRN Neurosci 2013;2013.
  18. Scott LV, Dinan TG. Vasopressin and the regulation of hypothalamic-pituitary-adrenal axis function: implications for the pathophysiology of depression. Life Sci 1998;62:1985-98. https://doi.org/10.1016/S0024-3205(98)00027-7
  19. Glaser R, Kiecolt-Glaser JK. Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 2005;5:243-51. https://doi.org/10.1038/nri1571
  20. Cohen S, Janicki-Deverts D, Doyle WJ, Miller GE, Frank E, Rabin BS, Turner RB. Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc Natl Acad Sci U S A 2012;109:5995-9. https://doi.org/10.1073/pnas.1118355109
  21. Medzhitov R, Horng T. Transcriptional control of the inflammatory response. Nat Rev Immunol 2009;9:692-703. https://doi.org/10.1038/nri2634
  22. Park JH, Cha HY, Seo JJ, Hong JT, Han K, Oh KW. Anxiolytic-like effects of ginseng in the elevated plus-maze model: comparison of red ginseng and sun ginseng. Prog Neuropsychopharmacol Biol Psychiatry 2005;29:895-900. https://doi.org/10.1016/j.pnpbp.2005.04.016
  23. Choi JY, Woo TS, Yoon SY, Ike Campomayor Dela P, Choi YJ, Ahn HS, Lee YS, Yu GY, Cheong JH. Red ginseng supplementation more effectively alleviates psychological than physical fatigue. J Ginseng Res 2011;35:331-8. https://doi.org/10.5142/jgr.2011.35.3.331
  24. Al-Harbi KS. Treatment-resistant depression: therapeutic trends, challenges, and future directions. Patient Prefer Adherence 2012;6:369-88.
  25. Xu C, Teng J, Chen W, Ge Q, Yang Z, Yu C, Yang Z, Jia W. 20(S)-Protopanaxadiol, an active ginseng metabolite, exhibits strong antidepressant-like effects in animal tests. Prog Neuropsychopharmacol Biol Psychiatry 2010;34:1402-11. https://doi.org/10.1016/j.pnpbp.2010.07.010
  26. Dong HS, Han C, Jeon SW, Yoon S, Jeong HG, Huh YJ, Pae CU, Patkar AA, Steffens DC. Characteristics of neurocognitive functions in mild cognitive impairment with depression. Int Psychogeriatr 2016;28:1181-90. https://doi.org/10.1017/S1041610216000314
  27. Van Kampen JM, Baranowski DB, Shaw CA, Kay DG. Panax ginseng is neuroprotective in a novel progressive model of Parkinson's disease. Exp Gerontol 2014;50:95-105. https://doi.org/10.1016/j.exger.2013.11.012
  28. Churchill JD, Gerson JL, Hinton KA, Mifek JL, Walter MJ, Winslow CL, Deyo RA. The nootropic properties of ginseng saponin Rb1 are linked to effects on anxiety. Integr Physiol Behav Sci 2002;37:178-87. https://doi.org/10.1007/BF02734180
  29. Lovibond PF, Lovibond SH. The structure of negative emotional states: comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behav Res Ther 1995;33:335-43. https://doi.org/10.1016/0005-7967(94)00075-U
  30. Clarke DM, Currie KC. Depression, anxiety and their relationship with chronic diseases: a review of the epidemiology, risk and treatment evidence. Med J Aust 2009;190:S54-60.
  31. Kim JH. Cardiovascular diseases and Panax ginseng: a review on molecular mechanisms and medical applications. J Ginseng Res 2012;36:16-26. https://doi.org/10.5142/jgr.2012.36.1.16
  32. Backe EM, Seidler A, Latza U, Rossnagel K, Schumann B. The role of psychosocial stress at work for the development of cardiovascular diseases: a systematic review. Int Arch Occup Environ Health 2012;85:67-79. https://doi.org/10.1007/s00420-011-0643-6
  33. Lee CH, Kim JH. A review on the medicinal potentials of ginseng and ginsenosides on cardiovascular diseases. J Ginseng Res 2014;38:161-6. https://doi.org/10.1016/j.jgr.2014.03.001
  34. King Jr JT. Epidemiology of aneurysmal subarachnoid hemorrhage. Neuroimaging Clin N Am 1997;7:659-68.
  35. Rastogi V, Santiago-Moreno J, Dore S. Ginseng: a promising neuroprotective strategy in stroke. Front Cell Neurosci 2014;8:457.
  36. Nguyen CT, Luong TT, Kim GL, Pyo S, Rhee DK. Korean Red Ginseng inhibits apoptosis in neuroblastoma cells via estrogen receptor beta-mediated phosphatidylinositol-3 kinase/Akt signaling. J Ginseng Res 2015;39:69-75. https://doi.org/10.1016/j.jgr.2014.06.005
  37. Kumano H. [Osteoporosis and stress]. Clin Calc 2005;15:1544-7.
  38. Siddiqi MH, Siddiqi MZ, Ahn S, Kang S, Kim YJ, Sathishkumar N, Yang DU, Yang DC. Ginseng saponins and the treatment of osteoporosis: mini literature review. J Ginseng Res 2013;37:261-8. https://doi.org/10.5142/jgr.2013.37.261
  39. Kim HA, Kim S, Chang SH, Hwang HJ, Choi YN. Anti-arthritic effect of ginsenoside Rb1 on collagen induced arthritis in mice. Int Immunopharmacol 2007;7:1286-91. https://doi.org/10.1016/j.intimp.2007.05.006
  40. Hedon F. Anxiety and erectile dysfunction: a global approach to ED enhances results and quality of life. Int J Impot Res 2003;15:S16-9.
  41. Kim TH, Jeon SH, Hahn EJ, Paek KY, Park JK, Youn NY, Lee HL. Effects of tissue-cultured mountain ginseng (Panax ginseng CA Meyer) extract on male patients with erectile dysfunction. Asian J Androl 2009;11:356-61. https://doi.org/10.1038/aja.2008.32
  42. de Andrade E, de Mesquita AA, Claro Jde A, de Andrade PM, Ortiz V, Paranhos M, Srougi M. Study of the efficacy of Korean Red Ginseng in the treatment of erectile dysfunction. Asian J Androl 2007;9:241-4. https://doi.org/10.1111/j.1745-7262.2007.00210.x
  43. Surwit RS, Schneider MS, Feinglos MN. Stress and diabetes mellitus. Diab Care 1992;15:1413-22. https://doi.org/10.2337/diacare.15.10.1413
  44. Hong BN, Ji MG, Kang TH. The efficacy of red ginseng in type 1 and type 2 diabetes in animals. Evid Based Complement Alternat Med 2013;2013:593181.
  45. Yuan HD, Kim JT, Kim SH, Chung SH. Ginseng and diabetes: the evidences from in vitro, animal and human studies. J Ginseng Res 2012;36:27-39. https://doi.org/10.5142/jgr.2012.36.1.27
  46. Song SB, Tung NH, Quang TH, Ngan NT, Kim KE, Kim YH. Inhibition of TNF-alpha-mediated NF-kappaB transcriptional activity in HepG2 cells by dammarane-type saponins from Panax ginseng leaves. J Ginseng Res 2012;36:146-52. https://doi.org/10.5142/jgr.2012.36.2.146
  47. Chung KF, Marwick JA. Molecular mechanisms of oxidative stress in airways and lungs with reference to asthma and chronic obstructive pulmonary disease. Ann N Y Acad Sci 2010;1203:85-91. https://doi.org/10.1111/j.1749-6632.2010.05600.x
  48. Kullowatz A, Kanniess F, Dahme B, Magnussen H, Ritz T. Association of depression and anxiety with health care use and quality of life in asthma patients. Respir Med 2007;101:638-44. https://doi.org/10.1016/j.rmed.2006.06.002
  49. Maes M, Fisar Z, Medina M, Scapagnini G, Nowak G, Berk M. New drug targets in depression: inflammatory, cell-mediated immune, oxidative and nitrosative stress, mitochondrial, antioxidant, and neuroprogressive pathways. And new drug candidates-Nrf2 activators and GSK-3 inhibitors. Inflammopharmacology 2012;20:127-50. https://doi.org/10.1007/s10787-011-0111-7
  50. Hong CE, Lyu SY. Anti-inflammatory and anti-oxidative effects of Korean Red Ginseng extract in human keratinocytes. Immune Netw 2011;11:42-9. https://doi.org/10.4110/in.2011.11.1.42
  51. Wang Z, Li M, Wu WK, Tan HM, Geng DF. Ginsenoside Rb1 preconditioning protects against myocardial infarction after regional ischemia and reperfusion by activation of phosphatidylinositol-3-kinase signal transduction. Cardiovasc Drugs Ther 2008;22(6):443-52. https://doi.org/10.1007/s10557-008-6129-4
  52. Wang YG, Zima AV, Ji X, Pabbidi R, Blatter LA, Lipsius SL. Ginsenoside Re suppresses electromechanical alternans in cat and human cardiomyocytes. Am J Physiol Heart Circ Physiol 2008;295:H851-9. https://doi.org/10.1152/ajpheart.01242.2007
  53. Deng J, Lv XT, Wu Q, Huang XN. Ginsenoside Rg(1) inhibits rat left ventricular hypertrophy induced by abdominal aorta coarctation: involvement of calcineurin and mitogen-activated protein kinase signalings. Eur J Pharmacol 2009;608:42-7. https://doi.org/10.1016/j.ejphar.2009.01.048
  54. Lee JY, Lim KM, Kim SY, Bae ON, Noh JY, Chung SM, Kim K, Shin YS, Lee MY, Chung JH. Vascular smooth muscle dysfunction and remodeling induced by ginsenoside Rg3, a bioactive component of ginseng. Toxicol Sci 2010;117:505-14. https://doi.org/10.1093/toxsci/kfq201
  55. Shen LH, Zhang JT. Ginsenoside Rg1 promotes proliferation of hippocampal progenitor cells. Neurolog Res 2004;26:422-8. https://doi.org/10.1179/016164104225016047
  56. Fang F, Chen X, Huang T, Lue LF, Luddy JS, Yan SS. Multi-faced neuroprotective effects of ginsenoside Rg1 in an Alzheimer mouse model. Biochimi Biophys Acta 2012;1822:286-92. https://doi.org/10.1016/j.bbadis.2011.10.004
  57. Li JQ, Li ZK, Duan H, Zhang JT. [Effect of age and ginsenoside Rg1 on nitric oxide content and nitric oxide synthase activity of cerebral cortex in rats]. Yao Xue Xue Bao 1997;32:251-4.
  58. Xiong Y, Shen L, Liu KJ, Tso P, Wang G, Woods SC, Liu M. Antiobesity and antihyperglycemic effects of ginsenoside Rb1 in rats. Diabetes 2010;59:2505-12. https://doi.org/10.2337/db10-0315
  59. Quan HY, Yuan HD, Jung MS, Ko SK, Park YG, Chung SH. Ginsenoside Re lowers blood glucose and lipid levels via activation of AMP-activated protein kinase in HepG2 cells and high-fat diet fed mice. Int J Mol Med 2012;29:73-80.
  60. Kim M, Ahn BY, Lee JS, Chung SS, Lim S, Park SG, Jung HS, Lee HK, Park KS. The ginsenoside Rg3 has a stimulatory effect on insulin signaling in L6 myotubes. Biochem Biophys Res Commun 2009;389:70-3. https://doi.org/10.1016/j.bbrc.2009.08.088
  61. Gong YS, Chen J, Zhang QZ, Zhang JT. Effect of 17beta-oestradiol and ginsenoside on osteoporosis in ovariectomised rats. J Asian Nat Prod Res 2006;8:649-56. https://doi.org/10.1080/10286020500246063
  62. Huang Q, Gao B, Jie Q, Wei BY, Fan J, Zhang HY, Li XJ, Shi J, Luo ZJ, Yang L, et al. Ginsenoside-Rb2 displays anti-osteoporosis effects through reducing oxidative damage and bone-resorbing cytokines during osteogenesis. Bone 2014;66:306-14. https://doi.org/10.1016/j.bone.2014.06.010
  63. Liu T, Peng YF, Jia C, Yang BH, Tao X, Li J, Fang X. Ginsenoside Rg3 improves erectile function in streptozotocin-induced diabetic rats. J Sex Med 2015;12(3):611-20. https://doi.org/10.1111/jsm.12779
  64. Pyo MK, Park K-H, Oh MH, Lee H, Park YS, Kim NY, Park SH, Song JH, Park JD, Jung SH, et al. Ginsenoside Re enriched fraction (GS-F3K1) from ginseng berries ameliorates ethanol-induced erectile dysfunction via nitric oxide-cGMP pathway. Nat Prod Sci 2016;22:46-52. https://doi.org/10.20307/nps.2016.22.1.46
  65. Wang X, Chu S, Qian T, Chen J, Zhang J. Ginsenoside Rg1 improves male copulatory behavior via nitric oxide/cyclic guanosine monophosphate pathway. J Sex Med 2010;7:743-50. https://doi.org/10.1111/j.1743-6109.2009.01482.x
  66. Chen T, Xiao L, Zhu L, Ma S, Yan T, Ji H. Anti-asthmatic effects of ginsenoside Rb1 in a mouse model of allergic asthma through relegating Th1/Th2. Inflammation 2015;38:1814-22. https://doi.org/10.1007/s10753-015-0159-4
  67. Li LC, Piao HM, Zheng MY, Lin ZH, Choi YH, Yan GH. Ginsenoside Rh2 attenuates allergic airway inflammation by modulating nuclear factor-kappaB activation in a murine model of asthma. Mol Med Rep 2015;12:6946-54. https://doi.org/10.3892/mmr.2015.4272

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